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Non-calanoid copepods at the Bermuda Atlantic time-series (BATS) station

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Title:
Non-calanoid copepods at the Bermuda Atlantic time-series (BATS) station community structure and ecology, 1995-1999
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Book
Language:
English
Creator:
Al-Mutairi, Hussain Ali
Publisher:
University of South Florida
Place of Publication:
Tampa, Fla
Publication Date:

Subjects

Subjects / Keywords:
C: N-cycling
Trichodesmium
Macrosetella
Oncaea
Microzooplankton
Dissertations, Academic -- Marine Science -- Doctoral -- USF   ( lcsh )
Genre:
non-fiction   ( marcgt )

Notes

Summary:
ABSTRACT: Zooplankton were sampled on a monthly basis at the Bermuda Atlantic Time-series Study (BATS) site from January 1995 to December 1999. Samples were collected using a 1-m², 200 μm mesh net. The net sampled the water column in an oblique manner from the surface to a mean depth of 200 m. One day and one night tow from each cruise was examined microscopically to determine the community structure of the non-calanoid copepods. In addition, a three year set of nighttime samples were examined taken by 0.5-m², 20 and 35 μm mesh nets (1995-1996 and 1997, respectively) towed obliquely to 150 m. The dominant orders in terms of overall abundance were the Cyclopoida and Poecilostomatoida. The cyclopoid genus, Oithona, was most abundant followed by the Poecilostomatoid family, Oncaeidae, and the genera Farranula and Corycaeus. Harpacticoids, although common, were about an order of magnitude less abundant and were dominated by Macrosetella gracilis.Representatives of the Mormonilloida and Siphonostomatoida also were frequently encountered, although in much lower numbers. Overall, pronounced seasonal signals were noted; highest abundances occurred during spring and lowest during winter. However, abundance of some groups peaked either in the fall or winter, with lowest abundance in spring or summer. Miraciid copepods are estimated to consume an overall average of 359 μg C m⁻² d⁻¹ and regenerate 55 μg N m⁻² d⁻¹ derived from Trichodesmium at BATS. Highest grazing and regeneration rates were found in late summer through fall and early winter and lowest in spring and early summer. The ecological consequences of miraciid copepod feeding on Trichodesmium are discussed. The 20-35 μm net samples revealed an astonishing abundance of non-copepod species, some totally missed and others woefully under-sampled by the 200 μm net.At least four species of oncaeid copepods and the harpacticoid copepod Microsetella norvegica were found in abundances that were more than an order of magnitude higher than the corresponding numbers of non-calanoid copepods sampled by the 200 μm net. The role of all non-calanoid copepods, from both net systems, in C and N dynamics at BATS is analyzed and discussed along with the sex-ratios of most identified species.
Thesis:
Dissertation (Ph.D.)--University of South Florida, 2009.
Bibliography:
Includes bibliographical references.
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Mode of access: World Wide Web.
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System requirements: World Wide Web browser and PDF reader.
Statement of Responsibility:
by Hussain Ali Al-Mutairi.
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Title from PDF of title page.
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Document formatted into pages; contains 215 pages.
General Note:
Includes vita.

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University of South Florida Library
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University of South Florida
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All applicable rights reserved by the source institution and holding location.
Resource Identifier:
aleph - 002069356
oclc - 608290181
usfldc doi - E14-SFE0003215
usfldc handle - e14.3215
System ID:
SFS0027531:00001


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Non Calanoid Copepod s at the Bermuda Atlantic Time S eries Study (BATS) Station: Community Structure and Ecology, 1995 1999 b y Hussain Ali Al Mutairi A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy College of Marine Science University of South Florida Major Professor: Joseph Torres, Ph.D. Deborah Steinberg, Ph.D. David Mann, Ph.D. Kendra Daly, Ph.D. Ernst Peebles, Ph.D. Date of Approval: November 17 2009 Keywords: C: N cycling, Trichodesmium Macrosetella Oncaea microzooplankton Copyright 2009, Hussain Al Mutairi

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Dedication This work is dedicated to the people who mean the most to me my mother and father whose guidance built my character and my sisters Soraya and Suhaila who encouraged me to go on during the rough patches. Finall y and most importantly I dedicate this dissertation to my daughter s Norah, Alyah, and Amani It was to provide a better future for them that I took on the challenge of earning my Ph.D.

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Acknowledgements Numerous people and institutions have been instrumental in creation of this work and are too numerous to acknowledge individually here However, there are some that due to the magnitude of their contribution necessitate mention. Firstly, I would like to acknowledge my appreciation for the Kuwait Public Authority for Applied Education and Training for the opportunity to further my education by providing a full scholarship for 4 years. Additional funding came from the Bermuda Institute of Ocean Sciences (BIOS) for a 3 week stay at the BIOS institute in Bermuda. I am greatly indebted to m y supervisor Joseph Torres who took a chance by accept ing me as a student in his lab and for his understanding of my circumstances during the entire process and especially towards the end. Also, I am grateful to all my committee members for their expertis e and help. In particular I would like to thank Dr. Deborah Steinberg who allowed me to work on the archived BATS zooplankton samples. I would also like to take this opportunity to thank Dr. Michael Lomas for allowing me unfettered use of his laboratory wh ile working on the Taylor tows.

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Note to Reader Due to the discover y just prior to publication of this dissertation of a systematic error control involving an underestimation of volumes filtered for all BATS 200 m net samples, the reader should bear in mind that all copepod abundance results of chapters 2 and 3 should be multiplied by 0.82 to achieve the corrected values.

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i Table of Contents List of Tables ................................ ................................ ................................ ................................ ................ vi List of Figures ................................ ................................ ................................ ................................ .............. ix Abstract ................................ ................................ ................................ ................................ ...................... xiii Chapter One: Introduction ................................ ................................ ................................ ............................. 1 Background ................................ ................................ ................................ ................................ ..... 2 Organization ................................ ................................ ................................ ................................ .... 4 Chapter Two: BATS 200 m Net Non Calanoid C o pepod Community Structure: Diel, S easonal, Interannual Patterns and E cology ................................ ................................ ................................ ........... 6 Introduction ................................ ................................ ................................ ................................ ..... 7 M aterials and M ethods ................................ ................................ ................................ .................... 9 Shipboard Sample C ollection ................................ ................................ ........................... 9 Processing for Community Structure A nalysis ................................ ................................ 9 Metabolic E stimations ................................ ................................ ................................ .... 10 Est imation of Larvacean House C P roduction at BATS ................................ ................. 12 Ancillary BATS D ata ................................ ................................ ................................ ..... 13 Stati stical M ethods ................................ ................................ ................................ .......... 13 Results ................................ ................................ ................................ ................................ ........... 14 Net Tow D ata ................................ ................................ ................................ .................. 14 General Community C omposition ................................ ................................ .................. 15 Diel D ifferences ................................ ................................ ................................ ............. 19 Ann ual and Seasonal Patterns of Total Non Calanoid A bundance at BATS .................. 20 Oithona and Oncaea spp Annual and Seasonal T rends ................................ ................. 20 Corycaeus and Farranula spp Annual and Seasonal S tructure ................................ ..... 24 Seasonal and Annual T rends of Lubbokia spp ................................ ................................ 30

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ii Annual and Seasonal Community Structure of Sapphirinid C opepods .......................... 31 Patterns of Other Non Calanoid G roups at BATS ................................ .......................... 32 Non Calanoid Abundance Relationship to Environmental F actors ................................ 48 Primary Production and P igments ................................ ................................ .................. 48 Par ticulate Organic Carbon (POC) ................................ ................................ ................. 49 Role of Non Calanoid Copepods in C and N D ynamics at BATS ................................ .. 51 Feeding S trategies of Oithona spp and their Ecological S ignificance to the BATS A rea ................................ ................................ ................................ .............. 55 Ecological Role of the A ssociation of Oncaeidae with L arvacea n H ouses .................... 56 Discussion ................................ ................................ ................................ ................................ ..... 58 Comparison to Previous S tudies n ear BATS ................................ ................................ .. 58 Causes of Observed Seasonal and Annual Patterns in Community S tructure and A bundance ................................ ................................ ................................ ............... 61 Assumptions used in Estimating Consumption of Larvacean H ouse s by O ncaeid C opepods ................................ ................................ ................................ ................. 65 Sapphirina spp. Associations with S alps at BATS ................................ ......................... 68 Summary and C onclusions ................................ ................................ ............................. 69 Chapter Three: Harpacticoid Copepods of the Family Miraciidae: The Ecological C onsequences of t heir A ssociation with Trichodesmium spp. to the BATS R egion ................................ ........................ 71 Introduction ................................ ................................ ................................ ................................ ... 72 Materials and M et hods ................................ ................................ ................................ .................. 75 Sample Collection and P rocessing ................................ ................................ .................. 75 Biomass E stimates ................................ ................................ ................................ .......... 75 Carbon Specific Grazing R ates ................................ ................................ ....................... 76 Nitrogen Excretion R ates ................................ ................................ ................................ 77 As similation and C P ortioning ................................ ................................ ........................ 78 Trichodesmium C and N Standing Stock and P roduction at BATS ................................ 79 Statistical M ethods ................................ ................................ ................................ .......... 80

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iii Results ................................ ................................ ................................ ................................ ........... 81 Seasonal and Interannual Trends in Miraciid A bundance ................................ .............. 81 Relationship between M iraci id and Trichodesmium Colony A bundance ....................... 85 Miraciid Copepod G razing of Trichodesmium at BATS ................................ ................ 86 Trichodesmium C and N Standing Crop C onsumed ................................ ....................... 95 Nitrogen Excretion by Miraciid C opepods ................................ ................................ ..... 96 Discussion ................................ ................................ ................................ ................................ ..... 99 Validity of Assumptions U sed ................................ ................................ ........................ 99 Role of Trichodesmium and their Grazers in C and N B udgets at BATS ..................... 104 Summary and C onclusions ................................ ................................ ........................... 105 Chapter Four: BATS 64 200 m Size Category Zooplankton Community Structure: S easonal, Interannual P at terns and Ecology, with Emphasis on Non Calanoid C opepods ................................ 108 Introduction ................................ ................................ ................................ ................................ 109 Materials and M ethods ................................ ................................ ................................ ................ 111 Sample C ollection ................................ ................................ ................................ ......... 111 C ommunity Structure Analysis P rocessing ................................ ................................ ... 111 Estimates of Biomass and Carbon Nitrogen Cycling by M icrozooplankt on ................ 112 Estimation of Microsetella spp Carbon D emand ................................ ......................... 113 Statistical M ethods ................................ ................................ ................................ ........ 114 Results ................................ ................................ ................................ ................................ ......... 114 Tow S tatistics ................................ ................................ ................................ ............... 114 General Community S tructure ................................ ................................ ...................... 115 Annual T rends ................................ ................................ ................................ .............. 129 Seasonal P atterns ................................ ................................ ................................ .......... 130 Relationsh ip between Zooplankton Abundance and Environmental F actors ................ 132 Copepod Biomass in the 64 200 m Size F ractions ................................ ..................... 133 Microzooplankton C and N D ynamics at BATS ................................ .......................... 137 Aggregate C G razed by Microsetella spp at BATS ................................ ..................... 140

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iv Net Capture E fficiencies of the Two Net Types E mployed at BATS .......................... 141 Discussion ................................ ................................ ................................ ................................ ... 1 46 Comparisons with Previous Studies in the BATS V icinity ................................ .......... 146 The Oncaeid Microcopepod C ommunity at BATS ................................ ....................... 148 Assumptions Used in Estimating R ole of Microsetella spp at BATS .......................... 152 Summary and C onclusions ................................ ................................ ........................... 155 Ch apter Five: Sex Ratios of Non Calanoid C opepods at BATS (1995 1999) ................................ .......... 156 Introduction ................................ ................................ ................................ ................................ 157 Materials and M ethods ................................ ................................ ................................ ................ 159 Sample Collection and A nalysis ................................ ................................ ................... 159 Results ................................ ................................ ................................ ................................ ......... 160 BATS 200 m Net N on Calanoid Sex R atios ................................ .............................. 160 Taylor (64 200 m) Non Calanoid Copepod Sex R atios ................................ ............. 167 Discussion ................................ ................................ ................................ ................................ ... 169 Comparison of BATS Non Calanoid Sex Ratios to Previous S tudies .......................... 169 Reproductive Strategy Influence on Field Observed Sex R ati os in C opepods ............. 170 Role of Selective Predation in S haping Observed Copepod Sex R atios ....................... 171 Role of Sampling B ias ................................ ................................ ................................ .. 173 Possible Role of Sex Change on Sex R atios ................................ ................................ 174 Summary and C onclusions ................................ ................................ ........................... 175 Chapter Six: Overall Summary and C onclusions ................................ ................................ ...................... 177 References ................................ ................................ ................................ ................................ ................. 181 Appendices ................................ ................................ ................................ ................................ ................ 202 Appendix 1: Average (standard Deviation) range and coefficient of variation (%) of volumes filtered and depths of tows for all 200 m net samples analyzed (1995 1999) ................................ ................................ ................................ ......................... 203 Appendix 2: Summary of annual average abundance m 2 (0 200 m) including standard d eviation, coefficient of variation (%) and range for all genera (adults and

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v copepodites) of BATS 200 m non calanoid copepod genera ................................ ............ 204 Appendix 3: Summary of pooled seasonal average abundance m 2 (0 200 m) including s tandard d eviation, coefficient of variation (%) and range for all genera (adults and copepodites) of BATS 200 m non calanoid copepod genera ................................ ........... 206 Appendix 4: Summary of annual and seasonal average miraciid copepod abundance m 2 (0 200 m) including standard deviation, coefficient of variation (%) and range for all 200 m net samples at BATS (1995 1999) ................................ ................................ ......... 208 Appendix 5: General tow statistics (average, standard deviation, range and % coefficient of variation) for all 20 and 35 m n et samples analyzed (1995 1997) ................................ 209 Appendix 6: Annual non calanoid average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200 m size fractions) analyzed (1995 1997) ................................ ................................ .......................... 210 Appendix 7: Annual other zooplankton average abundance data (0 150 m) including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200 size m fra ctions) analyzed (1995 1997) ................................ ................................ ............ 211 Appendix 8: Seasonal non calanoid average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200 m size fractions) analyzed (1995 1997) ................................ ................................ .......................... 212 Appendix 9: Seasonal other zooplankton average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200 m size fra ctions) analyzed (1995 1997) ................................ ................................ ............ 213 Appendix 10: Overall, annual and seasonal respiratory carbon estimates of all copepod adult and larval stages for 64 200 m size fraction (0 150 m) of all Taylor tows at BATS ................................ ................................ ................................ ................................ ... 214 Appendix 11: Overall, annual and seasonal inorganic nitrogen excretion estimates of all copepod adult and larval stages for 64 200 m size fraction (0 150 m) of all Taylor tows at BAT S ................................ ................................ ................................ ....................... 215 About the Author ................................ ................................ ................................ .............................. End Page

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vi List of Tables Table 1 Selected non calanoid copepod taxa average abundance distributions and overall (geometric means) of individual biomass (dry weight) among various size classes at the HOT site ................................ ................................ ................................ .... 11 Table 2 Published daily rates of larvacean house production and C content of newly formed and discarded houses ................................ ................................ ................................ ...... 12 Table 3 BATS 200 m net samples: Nom calanoid copepod families and species enumerated with overall integrated abundance (m 2 0 200 m) and range plus seasons of maximum densities ................................ ................................ ................................ ......... 16 Table 4 Non calanoid copepod species with statistically significant differences in diel abundance using paired (60 day night pairs) sign ................................ .. 19 Table 5 Statistically significant (p < 0.05) differences between years for major BATS non calanoid copepods (200 m net samples) ................................ ................................ 21 Table 6 Statistically significant (p < 0.05) differences between pooled seasons f or major BATS non calanoid copepod s (200 m net samples) ................................ .................... 22 Table 7 Significant (p < 0.05) results of Spearman Rank correlation analysis of cruise averaged BATS 200m net non calanoid abundance and various biological parameters measured during same cruise integrated t o 200 m depth .............................. 49 Table 8 Seasonal, annual and overall carbon demand (CD) of bulk mesozooplankton as well as total non calanoids, including the top 3 most abundant genera and families at BATS ................................ ................................ ................................ ............ 52 Table 9 Seasonal, annual and overall Dissolved Inorganic Nitrogen Excretion (DINE) of bulk mesozooplankton as well as total non calanoids, including the top three most abundant genera and families at BATS ................................ ................................ .......... 53

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vii Table 10 Percentage o f primary production nitrogen demand met by non calanoid copepods and bulk zooplankt on nitrogen excretion at BATS ................................ ......................... 54 Table 11 Seasonal, annual and overall results of larvacean house carbon production as well as total non calanoid, Oncaeidae and Corycaeidae rates of house consumption at BATS ................................ ................................ ................................ .............................. 57 Table 12 Individual miraciid copepod biomass es timates from previous studies ................................ 76 Table 13 Published grazing rates of miraciid copepods ................................ ................................ ........ 77 Table 14 Published rates of nitrogen excretion for Macrosetella gracilis ................................ ............ 78 Table 15 Results of Spearman Rank analysis of cruise averaged miraciid copepod species and Trichodesmium colony abundance m 2 (0 200 m) for the period 1995 1997 concomitant and lagged miraciid data ................................ ................................ ............ 86 Table 16 Annual and seasonal Trichodesmium carbon grazed by miraciid copepods at BATS from 1995 to 1999 ................................ ................................ ............................... 92 Table 17 Annual and seasonal Trichodesmium nitrogen ingested by miraciid copepods at BATS from 1995 t o 19 99 ................................ ................................ ............................... 93 Table 18 Percentage of Trichodesmium carbon standing crop consumed by miraciid copepod species at BATS for the period 1995 1997 ................................ ................................ ..... 95 Table 19 Percentage of Trichodesmium nitrogen standing crop consumed by miraciid copepod species at BATS for the period 1995 1997 ................................ ................................ ..................... 96 Table 20 Trichodesmium nitrogen excreted by miraciid copepods at BATS for the period of 1995 to 1999 ................................ ................................ ................................ ................... 97 Table 21 Percentage of primary production (Integrated to 140m and assuming a C:N of 6.6) supported by miraciid copepod N e xcretion at BATS (1995 1999) ............................... 99 Table 22 Estimated biomass for the average constituent of each category and species of copepod present in the 64 200 m size category at BATS ................................ ......................... 112 Table 23 Taylor net zooplankto n (64 200m) taxa enumerated with overall mean individual abundance m 2 (0 150 m) and seasons of maximum numbers ................................ .............. 116 Table 24 200 m

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viii size fracti on zooplankton (1995 1997) ................................ ................................ ......... 129 Table 25 64 200 m size frac tion zooplankton (1995 1997) ................................ ...................... 132 Table 26 Significant (p < 0.05) results of Spearman Rank correlation analysis of abundance ( m 2 ) of selected zooplankton taxa from the Taylor (64 200 m) size fraction (0 150 m) and various biological parameters measured during the same cruise and integrated to 150 m at BATS (1995 1997) ................................ ............................. 133 Table 27 Larvacean hous e production (mg C m 2 d 1 ) and Microsetella spp. carbon demand (mg C m 2 d 1 ) for 64 200 m size fractions integrated to 150 m (1995 1997) ............ 140 Table 28 Percentage contribution of the > 200 and 64 200 m size fractions to total abundance m 2 of various non calanoid species for all Taylor tows analyzed (1995 1997) ........... 144 Table 29 Cruise averaged total and size fractionated biomass (mg dry weight m 2 0 150 m) form BATS and Taylor tows (1995 1997) ................................ ................................ .... 149 Table 30 Comparison between abu ndance (copepods m 2 ) of oncaeid microcopepods within the epipelagic (0 100) layer from the BATS region and previous studies .......................... 150 Table 31 Annual sex ratios expressed as percentage of total numbers of selected non calanoid species for 1995 19 99 BATS 200 m (0 200 m) net samples ................................ ...... 163 Table 32 Seasonal sex ratios expressed as percentage of total numbers of selected non calanoid species for 1995 1999 BATS 200 m net samples (0 200 m) ................................ ...... 165 Table 33 Sex ratios expressed as percentage of total numbers of selected non calanoid species for all Taylor tows (64 200 m size fractions, 0 150 m) analyzed (1995 1997) .......... 168

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ix List of Figures Figure 1 Cruise averaged total non calanoid copepod abundance m 2 (0 200 m) for all years analyzed (1995 1999) ................................ ................................ ................................ ..... 18 Figure 2 Cruise averaged Oithona spp (adults and copepodites) individual abundance m 2 (0 200 m) at BATS (1995 1999) ................................ ................................ ................... 25 Figure 3 Mean cruise individual abundance m 2 (0 200 m) of top two dominant specie s of Oncaea ( O. media and O. scottodicarloi ) at BATS (1995 1999) ................................ ... 26 Figure 4 Cruise averaged individual abundance m 2 (0 200 m) of Oncaea mediterranea females and Oncaea spp. males (mixture of O. media O. scottodicarloi and O. mediterranea ) at BATS (1995 1999) ................................ ................................ .............. 27 Figure 5 Cruise averaged individual abundance m 2 (0 200 m) of Triconia conifera T. minuta and Oncaea venusta species at BATS (1995 1999) ................................ ........................ 28 Figure 6 Cruise averaged individual abundance m 2 (0 200 m) of Oncaea spp. copepodites at BATS (1995 1999) ................................ ................................ ................................ ......... 29 Figure 7 Cruise averaged individual abundance m 2 (0 200 m) of Corycaeus (sub genus Agetus ) at BATS (1995 1999) ................................ ................................ ................................ ..... 33 Figure 8 Cruise averaged individual abundance m 2 (0 200 m) for Cor ycaeus spp. (subgenus Corycaeus ) at BATS (1995 1999) ................................ ................................ .................. 34 Figure 9 Cruise averaged individual abundance m 2 (0 200 m) of the Corycaeus sub genus Onychocorycaeus at BATS (1995 1999) ................................ ................................ ........ 35 Figure 10 Cruise averaged individual abundance m 2 (0 200 m) of Corycaeus spp. of the sub genus Urocorycaeus at BATS (1995 1999) ................................ ................................ ... 36 Figure 11 Cruise averaged individual abundance m 2 (0 200 m) for Corycaeus spp. copepodites at BATS (1995 1999) ................................ ................................ ................................ ..... 37 Figure 12 Cruise averaged individual a bundance m 2 (0 200 m) of Farranula spp. at BATS

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x (1995 1999) ................................ ................................ ................................ .................... 38 Figure 13 Cruise averaged individual abundance m 2 (0 200 m) of Lubbokia squillimana ( adults and cop epodites) at BATS (1995 1999) ................................ ............................. 39 Figure 14 Cruise averaged individual abundance m 2 (0 200 m) of Sapphirina metallina and all other Sapphirina spp. ( including cop epodites) at BATS (1995 1999) ........................... 40 Figure 15 Cruise averaged individual abundance m 2 (0 200 m) of four most abundant Sapphirina spp after S. metalli na at BATS at BATS (1995 1999) ................................ 41 Figure 16 Cruise averaged individual abundance m 2 (0 200 m) of Sapphirina spp. 6 8 th most common species after S. metallina at BATS (1995 1999) ................................ .............. 42 Figure 17 Cruise averaged individual abundance m 2 (0 200 m) of Copilia spp. at BATS (1995 1999) ................................ ................................ ................................ .................... 43 Figure 18 Cruise averaged individual abundance m 2 (0 200 m) of less common Sapphirinid copepod genera Corisa and Vettoria at BATS (1995 1999) ................................ ........... 44 Figure 19 Cruise averaged individual abund ance m 2 (0 200 m) of Mormonilla minor (females) at BATS (1995 1999) ................................ ................................ ................................ ..... 45 Figure 20 Cruise averaged individual abundance m 2 (0 200 m) of less common genera from the families Rataniidae, Pontoeciellidae and Oncaeidae at BATS (19 95 to 1999) ............... 46 Fi gure 21 Cruise averaged individual abundance m 2 (0 200 m) of non Miraciid harpacticoids at BATS (1995 1999) ................................ ................................ ................................ ..... 47 Figure 22 Cruise averaged individual larvacean abundance m 2 (0 200 m) for both large and small (< 2 mm and > 2 mm tail leng th) size c ategories at BATS (1995 1999) ....... 50 Figure 23 Comparison between monthly averaged individual abundance m 2 (0 200 m) of non calanoid copepod taxa of Deevey (1971) and BATS (1995 1999) ................................ 60 Figure 24 Cruise averaged individual abundanc e m 2 (0 200 m) of Macrosetella gracilis and Oculosetella gracilis at BATS (1995 1999) ................................ ................................ ... 83 Figure 25 Cruise averaged individual abundance m 2 (0 200 m) of Miracia efferata and Distioculus minor at BATS (1995 1999) ................................ ................................ ........ 84 Figure 26 Cruise averaged individual abundance m 2 (0 200 m) of miraciid copepods and

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xi Trichodesmium colonies (from Orcutt et a l., 2001) at BATS (1995 1997) .................... 87 Figure 27 Cruise averaged individual abundance m 2 (0 200 m) of Macrosetella gracilis and Tricho desmium colonies (from Orcutt et a l., 2001) at BATS (1995 1997) .................... 88 Figure 28 Cruise averaged individual abundance m 2 (0 200 m) of Miracia efferta and Trichodesmium colonies (from Orcutt et a l., 2001) at BATS (1995 1997) .................... 89 Figure 29 Cruise av eraged individual abundance m 2 (0 200 m) of Oculosetella gracilis and Trichodesmium colonies (from Orcutt et a l., 2001) at BATS (1995 1997) .................... 90 Figure 30 Cruise averaged individual abundance m 2 (0 200 m) of Distioculus minor and Trichodesmium c olonies (from Orcutt et a l., 2001) at BATS (1995 1997) .................... 91 Figure 31 Integrated temperature (C) for various depth horizons at BATS (1995 1999) ................... 107 Figure 32 Copepod nauplii abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997) ................................ ................................ ................................ .. 118 Figure 33 Calanoid copepod abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ ................................ .................... 119 Figure 34 Oithona spp. abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997) ................................ ................................ ................................ ... 120 Figure 35 Corycaeid copepodite abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ ................................ .................... 121 Figure 36 Larvacean abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997) ................................ ................................ ................................ ....... 122 Figure 37 Microsetella spp. individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997) ................................ ................................ ................................ .................. 123 Figure 38 Oncaea zernovi and Spinoncaea ivlevi abundance, individuals m 2 (0 150 m) from 64 200 m size fr actio ns at BATS (1995 1997) ................................ .......................... 124 Figure 39 Triconia minuta and T. dentipes abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ .......................... 125 Figure 40 Oncaea atlantica and O. vodjanitskii abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ .......................... 126

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xii Figure 41 Oncaea scottodicarloi and Oncaea spp. (male) abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ .................. 127 Figure 42 Oncaeidae copep odite abundance, individuals m 2 (0 150 m) from 64 200 m size f ractions at BATS (1995 1997) ................................ ................................ .................... 128 Figure 43 Biomass (dry weight) distributions among all 5 BATS size fractions (0 150 m) and estimates for (0 150 m) 64 200 m Taylor fraction (1995 1997) ................................ 134 Figure 44 Percent contribution of main species and groups to overall copepod biomass (64 200m size fraction integrated to 150 m) at BATS for all Taylor tows (1995 1997) ................................ ................................ ................................ .................. 136 Figure 45 Percentage of primary production p otentially consumed to satisfy the C demand (a) as well as that supported by recycled N (b) from copepods in the 64 200 m and mesozoop lankton > 200 m (1995 1997) ................................ ................................ ..... 138 Figure 46 Percent contribution of main species and groups to overall copepod C and N metabolism (64 200m size fraction integrated to 150 m) at BATS for all Taylor tows (1995 1997) ................................ ................................ ................................ .................. 139

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xiii Non Calanoid Copepods at the Bermuda Atlantic Time series Study (BA TS) Station: Community Structure and Ecology, 1995 1999 Hussain Al Mutairi ABSTRACT Zooplankton were sampled on a monthly basis at the Bermuda Atlantic Time series Study (BATS) site from January 1995 to December 1999. Samples were collected using a 1 m 2 sampled the water column in an oblique manner from the surface to a mean depth of 200 m. One day and one night tow from each cruise was examined microscopically to determine the community structure of the non calanoid copepods. In addition, a three year set of nighttime samples were examined taken by 0.5 m 2 1996 and 1997, respectively) towed obliquely to 150 m. The dominant orders in terms of overall abundance were the Cyclopoida and Poecilostomatoida The cyclopoid genus, Oithona was most abundant followed by the Poecilostomatoid family, Oncaeidae and the genera Farranula and Corycaeus Harpacticoids, although common, were about an order of magnitude less abundant and were dominated by Macrosetella gracilis Representatives of the Mormonilloida and Siphonostomatoida also were frequently encountered, although in much lower numbers. Overall, pronounced seasonal signals were noted; highest abundances occurred during spring and lowest during winter. Howe ver, abundance of some groups peaked either in the fall or winter, with lowest abundance in spring or summer. Miraciid copepods are estimated to consume an overall average of 359 g C m 2 d 1 and regenerate 55 g N m 2 d 1 derived from Trichodesmium at BATS. Highest grazing and regeneration rates were found in late summer through fall and early winter and lowest in spring and early summer. The ecological consequences of miraciid copepod feeding on Trichodesmium are discussed. The 20 35 revealed an astonishing abundance of non copepod species, some totally missed and others woefully under net. At least four species of o ncaeid

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xiv copepods and the harpacticoid copepod Microsetella norvegica were found in abundances that w ere more than an order of magnitude higher than the corresponding numbers of non calanoid copepods sampled by The role of all non calanoid copepods, from both net systems, in C and N dynamics at BATS is analyzed and discussed along with the sex ratios of most identified species.

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1 Chapter One Introduction

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2 Background The US Joint Global Ocean Flux Study (JGOFS) program was formed to better understand global program, two time series sites were initiated in 1988: th e Bermuda Atlantic Time series Study (BATS) in series (HOT) at station ALOHA (22 goal of the two stations was to investigate biogeochemical fluxes on seasonal as well as decadal time scales. The BATS time series station has continued to operate even after the ending of the JGOFS program in 2003 and is now under the direction of the Bermuda Institute of Ocean Sciences ( BIOS ) As part of the BATS program, zooplankton samples have been collected monthly beginning in April 1994 and have continued the present time. Previous analysis of the zooplankton samples included biomass but not community st ructure. The aim of present study is to contribute to the knowledge of BATS zooplankton species composition and ecology by analyzing the non calanoid copepod component. Non calanoid copepods represent a much under studied and under sampled category of cope pods due in part due to their small size and the difficulty of identification ( Turner, 2004; Bttger Schnack et al. 2004 and 2008) In addition, nets used to routinely sample zooplankton have mesh sizes m ) that vastly under sample many species and developmental stages of non calanoid copepods (Hopcroft et al 2001). Furthermore, several groups of non calanoids have unique associations with suspended aggregates of organic debris including abandoned larvacean houses (Alldredge 1977; Outsuka et al., 1 996 ; Steinberg et al., 1997 ) and colonies of Trichodes mium Copepods have long been recognized as a major component of zooplankton, both in terms of abundance and biomass ( McGowan and Walker, 1985, Longhur st, 1985; Landry et al., 2001) and by extension have a large impact on biogeochemical cycling of elements, particularly on sinking fluxes through production of fecal pellet and molts ( Small et al., 1983; Longhurst, 1991) and active transport of elements b y diel migrating species (Steinberg et al., 2000 and 2002 ; Al Mutairi and Landry, 2001) In addition, copepods serve as important secondary producers linking primary production to higher trophic levels in productive regions and transferring microbial loop production to larger animals in more

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3 oligotrophic systems ( Zhang et al., 1995 ; Calbet, 2001) However, the vast majority of population and ecological studies of copepods focused on one order (calanoida) and little attention has been paid to other free liv ing pelagic copepod orders. In addition to the known environmental impac ts of copepods discussed above, many non calanoid copepod groups have important associations that set them apart from most calanoid species. These include the ability to utilize sinking organic aggregates as a habitat and food source and in some cases as a nursery It is this ability to consume, and thereby recycle and repackage suspended aggregates of organic matter, which renders these animals important in open ocean ecology and biogeochemistry. Examples include the dependence of the harpacticoid family Miraciid ae on Trichodesmium colonies for food and as a nursery the Poecilostomatoid family O ncaeid ae and harpacticoid genus Microsetella associations with and feeding on discarded larvacean houses (Alldredge, 1972; Ohtsuka et al., 1996). These associations can have important impacts on pelagic elemental cycling and trophic transfer. For example, miraciid copepods are one of the few metazoa n consumers of Trichodesmium this is due to the toxic effect it has on most other zooplankton thus, rendering its production largely unavail able directly to other zooplankton (Hawser et al., 1992). However, miraciid species readily consume Trichodesmium making its organic C and N available other zooplankters, through predation by larger zooplankton as well as support ing primary production of other phytoplankton species by excreting consumed Trichodesmium N In addi tion, s pecies of the family O ncaeid ae and genus Microsetella are able to short circuit the microbial loop by directly consuming nanoplankton, and perhaps even bacteria caught on the filters of the larvacean houses they feed on (Ohtsuka et al ., 1996). These small particles would not normally be available to such large sized animals Furthermore in addition to direct consumption, the previously mentioned non calanoid groups can impact particle degradation through physical disruption of larger aggregates int o smaller particle with longer residence times in the warmer epipel a gic zones allowing further microbial breakdown (Steinberg et al., 1997; Goldthwait et al., 2004) Finally, non calanoid copepods dominate what is termed microcopepods (~ 500 m in body len gth or less). These include the harpacticoid genus, Microsetella and many species of Oncaeidae (B ttger

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4 Schnack, 2002; 2003; Uye and Onbe, 2002). In fact some of these species are too small to be captured at all by standard mesozooplankton mesh sizes 200 m). Due to their numerical importance and occasional biomass and productio n dominance, micro copepods play a pivotal role in the energy transfer to higher trophic levels, as well as in the transformation, transport and cycling of elements in t he ocean. Thus, analysis of their community structure and estimation of their role in biogeochemical cycling at BATS was a nother important goal of this study Organization The dissertation is composed of four main parts representing community structure of non calanoid copepods sampled from plankton net tows taken at the BATS site using two different net systems from 1995 to 1999 in the case of the 200 m net system and 1995 to 1997 for the smaller mesh net sam ples (20 35 m). In addition, metabolic calculations were carried out aimed at understanding the role of non calanoids in the C and N budgets of the BATS. Finally, sex ratios of non calanoid copepods were examined and possible causes of observed ratios are discussed. Specifically, c hapter two deals with non calanoid community structure of the 200 m net samples from the upper 200 m of the water column over a 5 year period (1995 to 1999). In addition, to the role in C and N dynamics that was estimated by ca lculating metabolic rates using abundance data from the present study and published metabolic equations of all n on calanoid groups and compares the results with estimates from total zooplankton, as well as examining the C demand of onca ei d copepods to larvacean house production estimated from larvacean abundance from the present study and published house production rates. In chapter three the association of members of the harpacticoid copepod family Miraciid ae with colonies of the Cyanob acteria Trichodesmium is examined. This was accomplished by utilizing miraciid abundance from the present study along with published grazing and N excretion rates of miraciid copepods and comparing these rates to published Trichodesmium colony C and N stan ding crops estimated during BATS cruises for a three year period (1995 1997) making cruise by cruise comparisons possible

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5 Chapter four deals with the copepod community structure of the 64 200 m size fractions separated out from the 20 and 35 m net sam ples. In addition, biomass, as well as C demand and N regeneration is calculated Results of biomass and C demand and N excretion of the 64 200 m size fractions are compared to those of the > 200 m size category. In addition the role of Microsetella spp in larvacean house consumption is examined. Lastly, the net capture efficiency of the different nets used at BATS (i.e. 200 vs. 20 and 35 m) is investigated Finally, chapter 5 presents data on the sex ratios of non calanoid s pecies from both the 200 a nd 20 35 m net sample s from the BATS site Results are compared to previous studies of non calanoid sex ratios and possible causes of observed ratios are discussed.

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6 Chapter Two BATS 200 m Net Non Calanoid Copepod Community Structure: Diel, Seasonal, Interannual Patterns and Ecology

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7 Introduction An important driver of oceanic biogeochemical cycling is the biota. In fact, the maintenance of the geochemical disequilibrium of carbon on earth is the result of a myriad of comparatively small biological export processes in the ocean known collectively a s the biological pump. Longhurst (1991) broke the biological pump down into three components. The first he likened to a rotary pump, by which materials are recycled in the euphotic zone (e.g. excretion and respiration). The second component was described a s an Archimedean pump, which represented the downward gravitational fluxes of materials from the surface layers of the ocean (e.g., fecal pellets, molts, larvacean houses and phytoplankton aggregates). The third and final component was described as a recip rocating pump, which represented the material actively exported out of the photic zone by diel migratory zooplankton. Mesozooplankton (> 200 m) have a role in all three elements of the biological pump. They produce compact fast sinking fecal pellets that contribute to gravitational fluxes (Paffenh fer and Knowles, 1979; Small et al., 1983). In addition, they augment recycling by excreting nitrogen and other nutrients in the photic zone (Legendre and Rivkin, 2002; Zhang et al. 1995). Lastly, zooplankton c an actively transport elements out of the upper layers of the water column by excreting material at depth (typically 300 600 m) which originated from the euphotic zone ocean (Longhurst et al., 1989; Steinberg et al., 2000 and Al Mutairi and Landry, 2001). Zooplankton play only a minor role in recycling in the euphotic zone compared to the smaller animals (micro and nanozooplankton), but they dominate passive as well as active elemental fluxes. Copepods are often the most important component of the zo oplank ton, generally comprising > 70% of the total standing stock (Omori and Ikeda, 1984). They are, therefore, the dominant players in the passive and active transport of elements in the ocean. Most ecological and biological studies of copepods have focused on the calanoids and much of what we know about pelagic copepod biology and ecology is skewed towards them. However, the paucity of studies of free living pelagic non calanoid copepods (orders Cyclopoida, Harpacticoida, Poecilostomatoida, Siphonostomatoida an d Mormonilloida) is not in keeping with their importance in the marine pelagic system. In fact, the family Oithonidae and Oncaeidae may be the most numerous metazoans on earth (B ttger Schnack 1996; Gallienne and Robins 2001; Hopcroft et al.,

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8 2001). Moreov er, Oithona similis alone has been described as the most widely distributed and abundant metazoan species on earth (Nishida, 1985). As previously mentioned members of the family Oncaeidae associate with and feed on larvacean houses. Larvaceans secret complicated mucus structures use d to filter small particles (generally 20 0.2 m) from the surrounding water W hen the filters become clogged, or when the animal is disturbed, the house is abandoned and a new one is quickly formed to repl ace it (Alldredge 1972 and Alldredge 1976). Some studies have shown that appendicularians may be capable of ingesting particles less than 0.2 m including sub micrometer colloidal organic matter (Flood et al., 1992) and viruses (Gowing, 1994) in the sea. Thus, it seems likely that appendicularians can influence particulate carbon distributions in the oceans of a wide size range. This has profound implications to oligotrophic oceanic systems known to be dominated by the microbial loop rather than the class ical diatom to fish food chains of more productive regions. Hence directly and making their production available to larger metazoans (e.g. copepods and smal l fish) by way of direct predation and through the production of houses that frequently have a large amount of attached food particles as well as fecal pellets produced by the larvacean. By virtue of their numerical importance to the zooplankton community in many areas they are second to copepods in abundance and their high growth rates, including high rates of house production, larvaceans are perhaps the most important zooplankton contributor to marine snow formation (Alldredge 1976). By associating with and feeding on abandoned larvacean houses oncaeid copepods contribute to the remineralization of a large portion of marine snow, particularly in oligotrophic systems such as the BATS site. The abundan ce, community structure and the impact on C and N cycli ng by non calanoid copepo ds, overall and the impact of oncaei ds on abandoned larvacean houses at BATS will be examined from monthly cruises from 1995 to 1999.

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9 Materials and M ethods Shipboard sample c ollection Zooplankton were collected at the BATS monthly basis (January 1995 December 1999), with occasional biweekly sampling during the months of January April. Samp ling was conducted employing a 1 m 2 rectangular net with 202 m mesh (Madin et al., 20 01). Replicate day and night tows were made to a target depth of 200 m. The net was fitted with a flow meter (General Oceanics), as well as a time, temperature and depth recorder (Vemco Minilog recorder) from June 1995 onwards. Prior to June 1995, depth wa s estimated from the wire out and the wire angle. Volume filtered was estimated from the flow meter counts and the mouth area of the net corrected to an effective mouth area. The effective mouth area was based on measurements of the angle of the net frame under average towing conditions and resulted in a 2% decrease of nominal mouth area. Non calanoid copepod abundance per cubic meter was calculated by dividing raw counts by the fraction of tow analyzed to arrive at the total abundance in the tow. The estim ated abundance in the entire tow was then divided by the calculated volume filtered during the particular tow to obtain the abundance per cubic meter of water. Depth integrated abundance data was normalized to a 200 m depth by multiplying the abundance m 3 by 200. Zooplankton from the tows were split into two parts with one part wet sieved to produce 5 nominal size classes of > 5, 5 2, 2 1, 1 0.5 and 0.5 0.2 mm and immediately flash frozen for biomass determinations. The other half was used to make a silho uette photograph and then preserved in a 5% buffered formalin seawater solution. Proc essing for community structure a nalysis Varying fractions of the preserved sample were used to make abundance estimates of the non calanoid copepods, as well as larvac eans. Most samples used in this study had been previously wet sieved through a 2 mm screen for an unrelated study. The remaining preserved sample was split using a Folsom

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10 splitter to obtain a fraction that was reasonable to count and contained at least 100 individuals of the dominant family, almost always members of Oithonidae or Oncaeidae. An overall average of 1/36 of the entire tow was analyzed (range 1/16 1/256). The average number of non calanoid copepods in the 131 tows examined was 869 (range 195 2,575) and 219 in the case of larvaceans (range 9 1,231). Samples were counted using a stereo microscope with up to 40 x magnification. Non calanoid copepods were identified to the genus level for all early stage copepodites, as well as Oithona spp. a dults, and to the species level for all other genera. The Poeciliostomatid genus Oncaea spp. and the harpacticoid family Miraciid ae were identified according to the classification of Huys and Bttger Schnack (1996) and Huys and Bttger Schnack (1994), resp ectively. Males and females were counted separately for each species identified, with the exception of male Oncaea media O. scottodicarloi and O. mediterranea which were not distinguished as and counted as a group. Separating the males of those species proved to be difficult. In addition, Microsetella rosea and M. norvegica were not separated into male and female as the features to distinguish the sexes were too small to be seen under the stereo microscope. Metabolic estimations C arbon demands and nit rogen excretion rates of the main genera as well the total non calanoid community enumerated at BATS were approximated using the metabolic equations of Ikeda (1985). Carbon demand was determined by estimating respiration rates and assuming that it made up 40% of ingested carbon (Roman et al., 2002) with the remainder equally divided between production and egestion. Respiration rates were calculated using the Ikeda equation: Ln RO = 0.251 + 0.789 ln DWT + 0.049 T Where RO is l O 2 animal 1 h 1 DWT = dry w eight animal 1 in mg and T is average temperature in C for the upper 200m at BATS. RO was converted to respiratory carbon (RC) accordi ng to the following formula: RC = RO x RQ x 12/22.4, where RQ (respiratory quotient) is the molar ratio of carbon produce d to oxygen cons umed and was assumed to equal 1 In addition, nitrogen excretion rates were estimated using the following equation of Ikeda: Ln E = 2.890 + 0.762ln DWT + 0.051 T

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11 Individual copepod biomasses used in the above equations were estimated usin g the methods of Landry et al., (2001). Briefly, m ajor genera of non calanoid copepods were assigned proportional distributions among the various size classes utilizing the data of Landry et al., (2001). This was done by noting the overall proportion of the various non calanoid genera abundances retained in the different size fractions (preserved samples from the HOT site were size fractionated prior to community analysis of the zooplankton) and assigning them individual biomasses calculated by dividing a verage dry weight (200 tows) by average abundance (144 tows) for each separate size category (HOT data set). This estimate of individual biomass was deemed reasonable as the zooplankton community structure of the HOT and BATS sites is relatively similar. T able 1 contains the abundance distributions among the different size classes of the main genera of non calanoid copepods at HOT as well as the average dry weight of individual animals in each size category. Table 1 Selected non calanoid copepod taxa aver age abundance distribution s and overall geometric means of individual biomass (dry weight) among various size classes at the HOT site Group/species Individual biomass (geometric mean) 200 500m 6.6 g ind 1 500 1000m 19.6 g ind 1 1000 2000m 108 g ind 1 2000 5000m 404 g ind 1 Copilia spp. 0 % 0 % 73.3 % 26.7 % Copilia mirabilis 19.5 % 40.9 % 39.6 % 0 % Copilia quadrata 14.3 % 39.4 % 46.3 % 0 % Total Copilia spp. 32.5 % 21.3 % 38.7 % 7.5 % Sapphirina spp. 45.5 % 45.5 % 9 % 0 % Corycaeidae 85.3 % 14.3 % 0.3 % 0 % Oithona spp 89.4 % 10.6 % 0 % 0 % Oncaea spp. 97.2 % 2.8 % 0 % 0 % Lubbokia spp. 66.5 % 33.5 % 0 % 0 % Macrosetella gracilis 57.4 % 41.6 % 1.0 % 0 % Clytemnestra scutellata 93.4 % 6.6 % 0 % 0 % Miracia efferata 56.9 % 43.1 % 0 % 0 % For total zooplankton, hourly results of respired carbon and excreted nitrogen were multiplied by the abundance of all zooplankton (biomass in size class/individual dry weight) in each size fraction then converted to daily rates by separately multiplying by 12 all day and night tows then adding the average of the daytime and nighttime results. This was done to avoid biases towards either day or night data. Non calanoid copepod carbon demand and nitrogen excretion were estimated sepa rately, in order to gain insight into the relative importance of the non calanoid copepods to bulk (total) mesozooplankton carbon and

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12 nitrogen dynamics at BATS. However, data were averaged without regard to when the tow was taken as no significant diel di fferences were detected among the three groups of non calanoid copepods analyzed here. Moreover, average daily bulk zooplankton nitrogen excretion rates in the upper 200 m of the water column were compared to the nitrogen demand of phytoplankton estimated by dividing primary production by 6.6 (C : N Redfield Ratio). Estimation of l arvacean house C production at BATS For the pres ent study house production was estimated using rates determined by Sato et al., (2003). They measured daily house renewal rates of at several different temperatures. In addition, they measured the carbon content of newly produced houses as well as discarded ones. Average rates of house production at three different temperatures (20, 2 3 and 26 C) along with mean carbon content of both newly formed and freshly discarded houses for 3 oceanic species of Oikopleura ( O. longicauda O. fusiformis and O. rufescens ) were used (Table 2) Table 2 Published daily rates of larvacean house produc tion and C content of newly formed and discarded houses Species houses d 1 (20, 23 and 26 C) g C (new house 1 ) g C (discarded house 1 ) O. longicauda (15.6, 21.2 and 23.6) 0.16 0.68 O. fusiformis (18.4, 23.6 and 27.3) 0.48 1.2 O. rufescens (3.5, 5.3 and 5.2) 1.6 3.9 These species were chosen as they represent the larvacean community at BATS and they had the most measured parameters at the widest temperature range of the Sato et al., (2003) study The average of the three rates determined at each of the three separate experimental temperature were multiplied by larvacean abundance determined in the present investigation according to the integrated cruise temperature of the upper 100 m that best matched the rate determined at either of 20, 23 or 26C. This depth integrated temperature was chosen as most of the larvacean population is thought to reside within the upper 100 m in

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13 oceanic systems (Tomita et al., 2003). Next, l arvaceans present in this study were enumerated by c ounting tails, either with or without the trunk attached. In addition, if a tail was damaged it was counted only if the terminal tip was intact. However, due to the high proportion of damaged specimens, identification of the species, genus or even family w as not attempted. Rather all individuals were grouped as the class Larvacea (Appendicularia). Ancillary BATS data Particulate organic carbon (POC) and nitrogen (PON) fluxes were measured in the BATS program as described in Steinberg et al., (2001) using procedures detailed in Michaels and Knapp (1996). Briefly, a free drifting surface tethered cylindrical sediment trap array was deployed approximately 9 km south of the BATS station. Primary production was measured in the upper 140 m of the water column via an in situ incubation array. Bottles were held at 8 depths (1, 20, 40, 60, 80,100,120 and 140 m) for the duration of the dawn to dusk 14 C uptake experiment. Phytoplankton chlorophyll was measured using both fluorometric and high performance liquid chr omatography (HPLC) methods, while accessory pigments (e.g. fucoxanthin, peridinin etc.) were analyzed using only HPLC. All data of the proceeding measurements were obtained from http://bats.bios.edu/bats and depth in tegrated to 200 m using the trapezoid method. Statistical m ethods Statistical analysis of all data was performed using STATISTICA software (StatSoft I nc.) All non calanoid abundance data and all ancillary BATS data (e.g. primary production, pigments, e tc.) were tested to determine if t heir distributions were normal using the one sample Kolmogorov Smirnov test for normality For all statistical tests used results were considered significant at = 0.05 level. Annual and seasonal comparisons of non calanoid copepods were made using the Kruskal Wallis

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14 (K W) test of medians (a non parametric analog of ANOVA). This was due to the fact that many group and species abundance data were not normally distributed. Log tra nsformations of these data did not increase normality in a significant number of these cases. In addition to the K W test, post hoc multiple comparisons of average ranks of all pairs in the group were employed to determine which pairs were signi ficantly di fferent (e.g. spring > winter and fall in a seasonal comparison). In the present study seasons are defined as follows: December 21 March 20 is winter, March 21 June 20 is spring, June 21 September 20 is summer, and September 21 December 20 is fall. Further more, seasonal abundance data was pooled form all five years before statistical analysis. This was reasonable as the seasonal pattern within years was similar (i.e. spring and summer > winter and fall). Diel patterns were examined by comparing data from pairs of day night tows. There were 60 such pairs for all non calanoid groups and species. The data were tested using the sign test (a non parametric analog of the t test for dependent variables). Finally, relationships between non calanoid copepod abund ance and various biological parameters ( e.g. primary production, chlorophyll a, etc.) were examined using the Spearman R analysis (a non parametric analog of the Pearson product moment correlation coefficient). Results Net tow data A total of 131 tows were analyzed for the present study with 25, 24, 30, 25 and 27 tows from 1995, 1996, 1997, 1998 and 1999, respectively. Seasonally, the samples analyzed were composed of 34 winter, 39 spring, 29 summer and 29 fall tows. A summary of annual and overall se asonal tow information is listed in Appendix 1. The overall mean of maximum depth of tow recorded was 194 m with a standard deviation (s.d) of 34. The volume filtered had a grand average of 619 m 3 (s.d = 265). The variability in depth of tow was less than that of volume filtered as evidenced by the higher coefficient of variation (17 and 43%, respectively).

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15 General community c omposition Analysis of all 200 m net samples revealed a BATS non calanoid copepod community consisting of 5 orders, 11 families, 20 genera, and 52 species. The first order, Cyclopoida, consisted of the family Oithonidae. The second order, Harpacticoida, contained the families Miraciid a e, Clytemnestridae and Ectinosomatidae. The third and fourth non calanoid orders found in the present study were the Siphonostomatoida, including the families Pontoeciellidae and Rataniidae the Mormonilloida with its only family Mormonillidae. Finally, the last order identified, the Poecilostomatoida, contained the majority of non calanoid species found at BATS and was represented by the families Sapphirinidae, Corycaeidae, Oncaeidae and Lubbokiidae. All families and species identified are listed in Table 3 along with the overall abundance and range for the entire 5 year data set analyzed, as well as the season(s) of greatest abundance. Of the families found at BATS, Sapphirinidae was the most speciose, with 4 genera and 20 separate species identified. Th is was followed by the family Corycaeidae, with 2 genera and 12 species present. The next most diverse family was Oncaeidae with a total of 8 species in 3 genera. Other families found to be present were, in order of importance, Oithonidae (identified to ge nus level only), Lubbokiidae represented by 2 species, Miraciid ae with 4 species, Ectinosomatidae containing 2 species, followed by Mormonillidae, Clytemnestidae, Pontoeiellidae and Rataniidae, all represented by a single species. Although composed of 20 i dentified genera, the majority of the 200 m net non calanoid copepods were composed of a relatively small group of very abundant genera that dominated the community through all years and seasons analyzed. The overall total mean integrated abundance of all non calanoid copepods, including copepodites, was 13,575 m 2 (s.d = 7,716). The genus Oithona and family Oncaeidae alone made up an overall average of 35.6 and 35.1% of total non calanoid copepod abundance, respectively. The next three most abundant gener a were Farranula Coryc ae us and Lubbokia Overall, they formed 14.2, 10.6 and 1.65% of total numbers. Thus, of the 20 genera of non calanoid copepods found at BATS over a 5 year period, over 70% of the abundance was accounted for by only 2 genera and more than

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16 95% by 5 genera. All other genera identified each made up less than 1% of the average abundance of non calanoid copepods enumerated from all 131 tows. Table 3 BATS 200 m net samples: Non calanoid copepod families and species enumerated with overal l integrated abundance ( m 2 0 200 m) and range plus seasons of maximum densities Family Species Overall abundance Average range Season(s) of maximum densities Miraciid ae Macrosetella gracilis 62 0 333 Winter and Fall Oculosetella gracilis 24 0 197 Winter Miracia efferata 12 0 167 Fall Distioculus minor 12 0 118 Winter Clytemnestridae Clytemnestra scutellta 16 0 167 Year round Ectinosomatidae Microsetella rosea 5 0 141 Summer Microsetella norvegica 2 0 122 Summer Sapphirinidae Sapphirina metallina 70 0 356 Spring and Fall S. intestinata <1 0 18 Summer and Fall S. angusta 5 0 392 Spring S. auronitens 3 0 98 Winter and Summer S. auronitens sinuicauda 1 0 27 Winter and Spring S. darwini 4 0 130 Spring S. gastrica 2 0 54 Fall S. lactens 1 0 38 Winter and Fall S. nigromaculata 8 0 196 Spring S. opalina 1 0 65 Spring S. ovolanceolata gemma 6 0 181 Spring S. stellata 5 0 115 Year round S. scarleta 1 0 152 Spring S. bicuspida <1 0 18 Spring Copilia mirabilis 3 0 84 Fall Copilia quadrata 11 0 119 Spring Copilia vitrea 4 0 87 Spring and Summer Lubbokiidae Lubbokia squillimana 223 0 784 Summer and Fall Lubbokia aculeat a 2 0 58 Spring Oncaeidae 985 0 5079 Spring 1044 0 10372 Spring 593 0 2052 Summer Mixed Oncaea 905 15 3382 Summer O. venusta 363 0 3633 Spring Triconia conifera 319 0 2561 Year round 40 0 1383 Summer T. dentipes 7 0 790 Summer 2 0 58 Summer and Fall Corycaeidae Corycaeus speciosus 33 0 357 Fall C. clause 49 0 466 Spring and Summer C. typicus 246 0 1182 Spring, Summer and Fall C. limbatus 145 0 503 Spring, Summer and Fall C. flaccus 72 0 338 Spring and Summer C. latus 28 0 321 Summer and Fall C. lautus 16 0 98 Spring C. furcifer 4 0 98 Summer C. giesbrechtii 86 0 874 Spring C. brehmi 94 0 1107 Spring

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17 Table 3 (continued) Family Species Overall abundance Average range Season(s) of maximum densities Farranula gracilis 620 0 3509 Summer and Fall F. rostrata 1307 0 9834 Spring Oithonidae Oithona spp. 4836 190 15261 Spring and Summer Rataniidae Rtania flava 5 0 84 Spring and Fall Pontoeciellidae Pontoecielia abyssicola 9 0 186 Fall Mormonillidae 32 0 372 Spring and Summer The most abundant species (adults only) identified were members of the genera Farranula and Oncaea ( Oithona spp. were not separated into species). Farranula rostrata and F. gracilis made up 9.63 and 4.56% of overall non calanoid abundance respectively, while Oncaea media O. scottodicarloi and O. mediterranea females composed 7.69, 7.25, and 4.37%, respectively. The category mixed Oncaea males made up 6.67% of total non calanoid numbers and this category w as made up of the males of the three previously mentioned female Oncaea Together, the previous 3 Oncaea species (both sexes) composed an average of 26% of overall total non calanoid abundance. Other species of Oncaea that dominated total numbers of non ca lanoid copepods at BATS were O. venusta and Triconia conifera (synonym O. conifera ); those species made up a total of 2.68 and 2.35%, respectively. The genera Corycaeus and Lubbokia contained the next most abundant group of species. Lubbokia squillimana Corycaeus typicus and C. limbatus comprised 1.64, 1.81 and 1.06% of all non calanoid copepods numbers, respectively. All other species constituted, on an overall basis, less than 1% of total non calanoid copepods enumerated in all samples examined from BA TS. Figure 1 shows cruise averaged total non calanoid copepod abundance m 2 for all years a nalyzed.

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18 Figure 1 Cruise averaged total non calanoid copepod abundance m 2 (0 200 m) for all years analyzed (1995 1999) 0 5,000 10,000 15,000 20,000 25,000 30,000 35,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Total non calanoid copepods

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19 Diel d ifferences Significant diel differences in abundance were found in two non calanoid species ( Triconia conifera and Distioculus minor ) and Corycaeus copepodites ( Table 4 ) The species that exhibited the strongest evidence of diel migration was the On caeid, Triconia conifera both m ales and females had mean nighttime numbers that were much greater than daytime averages. Another species of non calanoid copepod that the analysis suggested was a diel migrator was the m iraciid Distioculus minor However, u nlike the case of Triconia conifera the behavior was only seen in males. Corycaeus spp. copepodite abundance was significantly higher, on average, in the daytime than at night. Table 4 Non calanoid copepod species with statistically significant differences in diel abundance using paired (60 day night pairs) sign test that showed 15% or greater deviation from 1:1 night to day ratio. Species Overall day abundance m 2 (0 200 m) Overall night abundance m 2 (0 200 m) p value 2.58 7.69 0.016 89.48 211.12 << 0.00 1 102.77 242.93 << 0.00 1 Corycaeus copepodites 777.10 587.07 0.00 1 Several taxa had day night differences significant at about the p = 0.10 level. These are presented as suspected diel vertical migrators. They included Corycaeus limbatus males and Oncaea media females (p = 0.080 and 0.106, respectively) both of which had higher nighttime abundance. Triconia minuta females, on the other hand, showed the reverse pattern with a higher daytime average (p = 0.081). Finally, larvaceans, taken as group and separated in to 2 size classes, hinted at a diel pattern with small larvaceans (tail length < 2mm) having higher mean daytime abundance (p = 0.107) than night while the large size class of larvaceans displayed the reverse pattern, with nighttime numbers higher than day (p = 0.079).

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20 Annual and s easonal patterns of total non calanoid a bundance at BATS The abundance of total non calanoid copepods on average, were highest in 1995 and 1999 with 15,244 and 16,963 copepods m 2 respectively, as compared to 1996 and 1997 with abundances of 11,236 and 11,368 m 2 respectively. Abundance in 1998 was intermediate (13,140 m 2 ). Interannual differences were not statistically significant (K W, p = 0.207). Only seven taxa had signifi cant annual diffe rences (Table 5 ). Seasonal analysis of total non calanoid copepod abundance revealed an overall patter n with spring > summer > fall > winter corresponding to 18,363 (s.d = 7,778), 15,185 (s.d = 7,541), 10,605 (s.d = 4,550), and 9,241 (s.d = 6,527) Static ally significant differences were found between spring a nd both winter and fall (Table 6 ). Many more individual taxa (29) exhibited significa nt seasonal differences (Table 6 ) compared to an nual differences Annual average abundance of all major genera of non calanoids at BATS is presented in Appendix 2 while seasonal aver ages are exhibited in Appendix 3 Oithona and Oncaea spp. annual and seasonal t rends Most genera followed an annual abundance pattern si milar to total non calanoid copepod numbers, particularly the However, for some groups and species there were annual and seasonal patterns that deviated from the overall trend. The most abundant genus varied among years between Oithona and Oncaea (includin g Triconia ). 1995 and 1999 had an almost even split among the 2 main genera with Oithona and Oncaea having an annual mean of 5,821 and 5,583 animals m 2 in 1995 and an overall average of 5,989 and 5,881 individuals m 2 in 1999 for both Oithona and Oncaea respectively. The years 1996 and 1998 had, on average, more Oncaea than Oithona with 4,030 vs. 3,649 and 5,211 vs. 4,111 copepods m 2 respectively. That pattern was reversed in 1997. The year 1997 had significantly more Oithona than Oncaea on average, with a mean of 4,531 and 3,282 copepods m 2 No statistically significant differences were found between years for either Oithona or Oncaea as a group (K W, p > 0.05).

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21 Table 5 Statistically significant (p < 0.05) differences between years for major BA TS non calanoid copepods (200 m net samples) Family Species Annual difference p value Kruskal Wallis p value Oncaeidae 1995 > 1997 n.s 0.036 O. venusta 1995 > 1999 n.s 0.010 Corycaeidae Corycaeus spp. (all) 1999 > 1996 n.s 0.031 C. typicus 1999 > 1996 n.s 0.035 C. flaccus 1995 > 1997 0.002 0.005 Farranula gracilis 1999 > 1998 0.031 0.038 Mormonillidae 1997 > 1995 and 1999 n.s 0.003 Includes copepodites values specific to pairs of years n.s: not significant Total Oithona (Figure 2) densities exhibited strong seasonal signals in all years analyzed. Generally, spring and summer were greater than winter and fall with significant differences (K W, p < 0.001) detected between spring and both winter (M.C, p = 0.001) and fall (M .C, p = 0.004). The family Oncaeidae at BATS contained 8 species, four Oncaea spp. three Triconia spp. and one Pacos sp (Table 3). There were very few occurrences of statistically significant differences between years for any Oncaea species with only O scottodicarloi females (1995 > 1997) and Oncaea venusta (1995 > 1999) displaying them (Table 5 ). Seasonally, most species of oncaeid copepods had highest numbers in spring and lowest in winter and fall. Combined, oncaeid copepods showed a statistically significant abundance maximum in spring compared to winter and fall (Table 5 ). Oncaea media and O. scottodicarloi females (Figure 3) both had a spring abundance that was significantly higher than all other seasons (K W, p << 0.001). Spring numbers were tw ice as high as those in winter and over 4.5 and 2.5 greater than average fall and summer numbers, respectively for Oncaea media Oncaea scottodicarloi had spring abundance twice that of winter and over 3.5 and 1.5 times that in fall and summer, respectivel y (see Table 6 for statistical details).

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22 Table 6 Statistically significant (p < 0.05) differences between pooled seasons for major BATS non calanoid copepods (200 m net samples) Family Species Seasonal difference Multiple comparison p value Kruskal Wallis p value Sapphirinidae Sapphirina spp. (all) Spring > Winter 0.004 0.005 Sapphirina metallina Spring and Fall > Winter 0.015 and 0.029 0.008 Copilia spp. (all) Spring > Winter, Summer and Fall < 0.001, 0.003 and 0.008 0.001 Copilia mediterranea Spring > Winter, Summer and Fall 0.055, 0.002 and 0.031 0.002 Corissa parva Fall > Winter and Spring 0.002 and 0.047 0.001 Lubbokiidae Lubbokia squillimana Summer > Winter and Spring Fall > Winter and Spring All < 0.001 All < 0.001 < 0.001 Oncaeidae Oncaea spp. (all) Spring > Winter and Fall < 0.001 and < 0.001 < 0.001 Spring > Winter, Summer and Fall All < 0.001 < 0.001 Spring > Winter, Summer and Fall 0.001, 0.012 and <0.001 < 0.001 Spring and Summer > Winter 0.003 and < 0.001 < 0.001 Mixed Oncaea Spring and Summer > Winter 0.006 and 0.001 0.001 O. venusta Spring > Winter, Summer and Fall All < 0.001 < 0.001 Triconia Summer > Winter and Fall < 0.001 and 0.006 < 0.001 Corycaeidae Corycaeus spp. (all) Winter < Spring, Summer and Fall All < 0.001 < 0.001 Corycaeus speciosus Fall > Winter, Spring and Summer All < 0.001 < 0.001 C. clausi Winter < Spring, Summer and Fall <0.001, < 0.001 and 0.014 < 0.001 C. typicus Winter < Spring, Summer and Fall All < 0.001 < 0.001 C. limbatus Winter < Spring and Summer 0.011, 0.001 0.001 C. flaccus Winter < Spring, Summer and Fall < 0.001, 0.003 and 0.038 < 0.001 C. latus Summer > Winter and Spring Fall > Winter and Spring All < 0.001 All < 0.001 < 0.001 C. giesbrechtii Spring > Winter 0.013 0.011 C. brehmi Spring > Winter, Summer and Fall All < 0.001 < 0.001 Corycaeus copepodites Winter < Spring, Summer and Fall All < 0.001 < 0.001

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23 Table 6 (Continued) Family Species Seasonal difference Multiple comparison p value Kruskal Wallis p value Farranula (all) Winter < Spring, Summer and Fall Fall < Spring and Summer < 0.001, <0.001 and 0.014 0.013 and 0.012 < 0.001 Farranula gracilis Summer > Winter and Spring Fall > Winter and Spring All < 0.001 All < 0.001 < 0.001 F. rostrata Spring > Winter and Fall Summer > Winter and Fall < 0.001 and < 0.001 0.002 and < 0.001 < 0.001 Oithonidae Oithona spp. Spring > Winter and Fall 0.001 and 0.004 <0.001 Includes copepodites values specific to pairs of seasons Oncaea mediterranea females (Figure 4), on the other hand, had a slightly different seasonal pattern with peak numbers in summer and lowest v alues in winter. S ignificant ly higher abundance was found in spring and summer compared to winter and fall. The Oncaea spp male group ( O. scottodicarloi O. media and O. mediterranea ) had a seasonal abundance distribution with a spring summer maximum approximately twice that of winter (Figure 4) The next two oncaeid species in terms of importance O. venusta and Triconia conifera (Figure 5) had very different seasonal abundance patterns. Oncaea venusta had very pronounced seasonal signals with an overall spring average (887, s.d = 94) nearly 5 times that of winter and summer and almost 25 times greater than fall averages. This was in stark contrast to the very consisten t seasonal pattern exhibited by Triconia conifera whose abundance did not differ by m ore than 20% between any seasons The last two species of oncaeids were found in much lower numbers with Triconia dentipes observed in only 4 of the 131 tows examined The other species, T. minuta however, was found in higher numbers and showed significant differences between seasons with maximum abundance in summer and minimum abundance in winter and fall (> factor of 10 lower). Finally, Oncaea spp. copepodites (Figure 6) showed no statistically significant seasonal differences, although fall had an overall average abundance nearly half that of all other seasons (303 vs. 529 630, s.d. = 168 vs. 545 712).

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24 Corycaeus and Farranula spp. annual and seas onal s tructure Highest abundance s of both Farranula and Corycaeus w ere found in 1999 with 2,346 and 2,015 individuals m 2 respectively while lowest abundance for Corycaeus occurred in 1996 (1,146 individuals m 2 ) and in 1997 for Farranula (1,684 copepod s m 2 ) No statistically significant differences were detected among all years analyzed for Farranula but 1999 had significantly higher abundance than 1996 in the case of Corycaeus (Table 4). However, when the two species of Farranula were analyzed separately, it was found that while F. rostrata did not exhibit any significant annual differences, F. gracilis was significantly more numerous in 1999 compared to 1998 (Table 5). The two genera of Corycaeidae found at BATS, Corycaeus and F arranula both showed significant seasonal patterns that differed from those displayed by members of Oncaea Corycaeus as a whole, had similar numbers from spring to fall (all mean values within 15% of each other) however; winter abundance was less than h alf that of all other seasons examined (Appendix 3) Farranula showed a similar seasonal pattern with a winter minima and a spring and summer maxima. Only two species of Corycaeus had statistically significant annual differences (Table 4) represented by C typicus (1999 > 1997) and C. flaccus (1999 > 1996). However, seasonal analysis of the main Corycaeus species at BATS revealed several with statistically significant difference (Table 5). Corycaeus typicus (Figure 7) had average winter abundance that was a factor of 3 lower than any other season. Spring, summer and fall abundance were similar (all within 20% of each other). Winter was also significantly lower than all other seasons for both C. limbatus and C. flaccus (Figure 7) and C. clausi However, C. s peciosus (Figure 8) had a very different seasonal pattern, with overall fall numbers being highest, nearly 11 times the abundance of either winter or spring and over 3 times more than summer. This was the first deviation from the overall seasonal trend of Corycaeus as a genus. Other Corycaeus species (Figure 9) had slightly different seasonal patterns than the previously mentioned. For example C. giesbrechtii had significantly higher abundance in spring than summer (Table 5). C. brehmi also had highest abundance in spring but lowest densities were found in fall. C. latus on the other hand had significantly higher abundance in summer and fall than winter and spring (Table 5).

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25 Figure 2 Cruise averag ed Oithona spp adults and copepodites) individual abundance m 2 (0 200 m) at BATS (1995 1999 ). 0 2,000 4,000 6,000 8,000 10,000 12,000 14,000 16,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Oithona spp.

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26 Figure 3 Mean cruise individual abundance m 2 (0 200 m) of top two dominant species of Oncaea ( O. media and O. scottodicarloi ) at BATS (1995 1999) 0 1,000 2,000 3,000 4,000 5,000 6,000 7,000 8,000 9,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Oncaea scottodicarloi O.media

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27 Figure 4 Cruise averaged individual abundance m 2 (0 200 m) of Oncaea mediterranea females and Oncaea spp. males (mixture of O. media O. scottodicarloi and O. mediterranea ) at BATS (1995 1999) 0 500 1,000 1,500 2,000 2,500 3,000 3,500 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Oncaea mediterranea Mixed

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28 Figure 5 Cruise averaged individual abundance m 2 (0 200 m) of Triconia conifera T. minuta and Oncaea venusta species at BATS (1995 1999) 0 500 1,000 1,500 2,000 2,500 3,000 3,500 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Triconia conifera Oncaea venusta Oncaea minuta

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29 Figure 6 Cruise averaged individual abundance m 2 (0 200 m) of Oncaea spp. copepodites at BATS (1995 1999) 0 500 1,000 1,500 2,000 2,500 3,000 3,500 4,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Oncaeidae copepodites

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30 The two least abundant species of Corycaeu s at BATS, C. fucifer and C. lautus (Figure 10) tended to be more common during spring and least abundant during winter. Finally unidentified Corycaeus spp. copepodites (Figure 11) were almost as numerous as adults of this genus (666 vs. 774 copepods m 2 ) and their abundance tended to follow that of the genus as a whole in terms of annual (no significant differences) and seasonal patterns (Winters significant ly < all other seasons). Farranula spp exhibited perhaps the most interesting example of seasonal non calanoid copepod succession at BATS which is illustrated in Figure 12. Farranula rostrata had its lowest numbers in fall (259 animals m 2 s.d. = 235) fo llowed by just over double the abundance in winter (not significantly different). However, F. rostrata x) than that of winter (Table 5) In addition, summer, although less numerous than spring, was ov er 2.5 times greater than winter and almost a factor 6 higher than fall abundance. The pattern was shifted for F. gracilis It had its lowest numbers in winter and spring (113 and 148 individuals m 2 ) and highest abundance in summer and fall. Thus, while F arranula rostrata was at its ebb in terms of population number during the fall, F. gracilis was at its highest (1 294 animals m 2 ) and when F. rostrata was at its spring peak of 2 557 individuals m 2 F. gracilis was at a low point in terms of abundance. This shift meant that spring and fall had high numbers of only one species while winter was a season of low values and summers a time of high numbers for both F rostrata and F. gracilis Seasonal and annual t re nds of Lubbokia spp Of the two species of Lubbokia found at BATS L. squillimana and L. aculeatus the former made up 99% of overall abundance. There was no significant difference s detected among the years analyzed (1995 1999), however, pronounced seasonal signals were detected. Summer and fall average abundances were approximately a factor of 2 higher than either winter or spring for (Figure 13) and these differences were statistically significant (Table 5).

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31 Annual and seasonal community structure of s apphirinid copepods No significant annual differences were found for any individual species of Sapphirina or the genus as a whole, although 1996 was the year with highest abundance and 1997 the lowest (186 and 82 copepods m 2 respectively ; Figure 14 ). T he eight most common species of Sapphirina were analyzed for annual and seasonal trends. P ronounced seasonal differences existed for total Sapphirina and many of the component species. The genus Sapphirina as a whole was significantly more numerous in spr ing with almost twice the abundance of any other season ( 189 vs. 94 103 copepods m 2 ) When individual species were analyzed the same pattern was evident with a few differences. In the case of the dominant species Sapphirina metallina (Figure 14), spring w as the season of highest overall abundance followed by fall with significantly lower densities in winter ( 88 and 72 vs. 54 copepods m 2 for spring, fall, and winter, respectively). In general, the remaining seven species also had highest abundances in spr ing and lowest in winter (Figures 15 and 16) The next genus most abundant genus of Sapphirinidae found at BATS was Copilia This genus contained 4 species, 2 of w hich ( C. mediterranea and C. quadrata ) were abundant (Figure 17) Overall abundance for Copilia spp. was highest in 1996 and 1999 (77 and 78 copepods m 2 ) and lowest in 1997 and 1998 (37 and 47 copepods m 2 ). However, these differences were not statistically significant T he same pattern was evident for Copilia mediterranea and C. quadrata (F igure 17) the difference being that 1995 had similarly high numbers as 1996 and 1999. The other less common species, Copilia mirabilis and C. vitrea had different years of maximum abundance (1995 and 1999, respectively). Seasonally, the genus Copilia ha d significantly greater abundance in spring, over twice that of all other seasons, with C. mediterranea following the same pattern. Copilia quadrata had highest average abundance in spring and lowest in winter and fall ( Figure 17 ) The less common species, Copilia vitrea had maximum abundance in spring and summer while C. mirabilis had peak numbers in fall, although none of these were sta tistically significant The last members of the family Sapphirinidae were the species Corissa parva and Vettoria granul ose (Figure 18). 1998 was the year of highest C. parva abundance, about a factor of 2 higher than all

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32 other years. However, this was not statistically significant. Vettoria granulosa abundance was relatively stable over all years though much less common th an C. parva Seasonally, Corissa parva had a pattern of lower numbers in winter and spring and higher abundance in summer and fall with significant differences between fall and both winter and spring (Table 5) No seasonal pattern was detected for Vettor ia granulosa abundance. Patterns of other non calanoid g roups at BATS The six remaining families (10 species) of non calanoid copepods at BATS accounted for more than half the total number of families found, but had a combined overall abundance of just 1.32% of the total. Further, if the 4 species in the family Miraciid ae, ( discusse d in greater detail in chapter 3 ), are excluded the percentage drops to just over 0.5%. One species in the family Mormonillidae, Mormonilla minor (Figure 19) was consistently present in sufficient numbers to allow meaningful analysis. It was one of only a handful to exhibit statistically significant annual differences (1997 > 1995 and 1999 ; Table 4 ). In addition to annual trends seasonal abundance patterns were also evident. Spring and summer had highest overall abundance of Mormonilla minor (44 and 38 animals m 2 respectively) whereas minimal numbers occurred in winter and fall (20 and 23 individuals m 2 respectively ), however, these differences were not statistically significant The remaining groups and species of non calanoid copepods at BATS were found in relatively small numbers and had no clear annual or seasonal trends. The exception to this was Pontoecielia abyssicola of the family Pontoeciellidae which had hi gher average a bundance in fall at 18 individuals m 2 than winter with 4 copepods m 2 A nnual and seasonal average abundance data for the rare species encountered at BATS can be found in Appendix 2 and 3 while all data is graphically illustrated in Figures 20 and 21.

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33 Figure 7 Cruise averaged individual abundance m 2 (0 200 m) Corycaeus (sub genus Agetus ) at BATS ( 1995 1999 ) 0 200 400 600 800 1,000 1,200 1,400 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corycaeus (Agetus) typicus C. (A.) limbatus C. (A.) flaccus

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34 Figure 8 Cruise averaged individual abundance m 2 (0 200 m) for Corycaeus spp. (sub genus Corycaeus ) at BATS (1995 1999 ) 0 50 100 150 200 250 300 350 400 450 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corycaeus (Corycaeus) speciosus C. (C.) clausi

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35 Figure 9 Cruise averaged individual abundance m 2 (0 200 m) of the Corycaeus sub genus Onychocorycaeus at BAT S (1995 1999) 0 200 400 600 800 1,000 1,200 1,400 1,600 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corycaeus (Onychocorycaeus) giesbrechtii C. (O.) brehmi C. (O.) latus

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36 Figure 10 Cruise averaged individual abundance m 2 (0 200 m) of Corycaeus spp. of the sub genus Urocorycaeus at BATS (1995 1999 ). 0 10 20 30 40 50 60 70 80 90 100 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corycaeus (Urocorycaeus) lautus C. (U.) furcifer

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37 Figure 11 Cruise averaged individual abundance m 2 (0 200 m) for Corycaeus spp. copep odites at BATS (1995 1999) 0 200 400 600 800 1,000 1,200 1,400 1,600 1,800 2,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corycaeus spp. copepodites

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38 Figure 12 Cruise averaged individual abundance m 2 (0 200 m) of Farranula spp. at BATS (1995 1999 ) 0 1,000 2,000 3,000 4,000 5,000 6,000 7,000 8,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Farranula gracilis Farranula rostrata

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39 Figure 13 Cruise averaged individual abundance m 2 (0 200 m) of Lubbokia squillimana ( adults a nd copepodites) at BATS ( 19 95 1999 ) 0 100 200 300 400 500 600 700 800 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Lubbokia spp.

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40 Figure 14 C ruise averaged individual abundance m 2 (0 200 m) of Sapphirina metallina and all other Sapphirina spp. ( including copepodites) at BATS (1995 1999) 0 200 400 600 800 1,000 1,200 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Sapphirina metallina Other Sapphirina spp.

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41 Figure 15 Cruise averaged individual abundance m 2 (0 200 m) of four most abundant Sapphirina spp after S. metallina at BATS at BATS (1995 1999) 0 100 200 300 400 500 600 700 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Saphirina nigromaculata S. ovolanceolata gemma S. angusta S. stellata

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42 Figure 16 Cruise averaged individual abundance m 2 (0 200 m) of Sapphirina spp. 6 8 th most common species after S. metallina at BATS (1995 1999 ) 0 20 40 60 80 100 120 140 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Saphirina auronitens S. darwini S. gastrica

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43 Figure 17 Cruise averaged individual abundance m 2 (0 200 m) of Copilia spp. at BATS (1995 1999 ). 0 50 100 150 200 250 300 350 400 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Copilia mediterranea C. quadrata C. vitrea C. mirabilis

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44 Figure 18 Cruise averaged individual abundance m 2 (0 200 m) of less common Sapphirinid copepod genera Coris s a and Vettoria at BATS (1995 1999 ). 0 10 20 30 40 50 60 70 80 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Corissa parva Vettoria granulosa

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45 Figure 19 Cruise averaged individual abundance m 2 (0 200 m) of Mormonilla minor (females) at BATS (1995 1999) 0 50 100 150 200 250 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Mormonilla minor

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46 Figure 20 Cruise averaged individual abundance m 2 (0 200 m) of less common genera from the families Rataniidae, Pontoeciellidae and Oncaeidae at BATS (1995 to 1999) 0 20 40 60 80 100 120 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Rtania flava Pontoecielia abyssicola Pacos punctatum

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47 Figure 21 Cruise averaged individual abundance m 2 (0 200 m) of non Miraciid harpacticoids at BATS (1995 1999 ). 0 20 40 60 80 100 120 140 160 180 200 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) Clytemnestra scutellta Microsetella rosea Microsetella norvegica

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48 Non calanoid abundance r e lationship to environmental f actors In the present study an attempt was made to identify exogenous factors that influenced the abundance of non calanoid copepods at BATS. Among the factors were the biotic parameters listed below, that have potential to influence zooplankton abundance. It is worth noting that, ultimately, all the factors are controlled by physic al a nd chemical mechanisms. R elationships were analyzed using Spearman Rank correlations Cruise averaged abundance data (m 2 integrated to 200 m) of t otal non calanoid copepods along with the top 5 families (Oithonidae, Oncaeidae, Coycaeidae, Sapphirinida e and Miraciid ae) and larvacean abundance we re each separately compared to six environmental factors (Table 6). Primary production and p igments The first parameter thought to be an important influence on non calanoid copepod abundance was primary production. However, only total abundance and one family (Oncaeidae) showed significant relationships However, even the significant relations had relatively low R values ( Table 7 ). In addition to primary production various phytoplankton pigment concentrations were examined to see if they correlated with non calanoid abundance at BATS. Three pigments were analyzed; chlorophyll a, fucoxanthin, and peridinin. The first pigmen t, Chlorophyll a (a proxy for bulk phytoplankton abundance) showed significant correlation with abundance of only one non calanoid family (Oncaeidae) and larvaceans. In addition, fucoxanthin (an accessory pigment indicative of diatoms) had significa nt correlations with abundance of total non calanoids and the families Onc ae i dae, Sapphirinidae, and Miraciid ae. In addition the R values were some of the strongest of any of the correlations analyzed (0.44 in the case of Oncaeidae and 0.46 for Miraciid ae ). The last pigment analyzed, peridinin (an accessory pigment indicative of dinoflagellates) showed significant correlations with abundance of total non calanoids, Oncaeidae, Sapphirinidae and Oithonidae. However, the strengths of the relationships were lo wer than those found for fucoxanthin (Table 7 ).

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49 Table 7 Significant (p < 0.05) results of Spearman Rank correlation analysis of cruise ave raged BATS 200 m net non calanoid abundance and various biological parameters measured during same cruise integrated to 200 m depth. Environmental parameter Zooplankton taxa R value P value Primary production (mg C) n = 70 Total non calanoid copepods 0.30 0.010 Oncaeidae 0.39 0.001 Sediment trap POC (mg C m 2 d 1 ) n = 58 Larvaceans 0.38 0.003 Chlorophyll a (mg m 2 ) n = 69 Larvaceans 0.30 0.011 Oncaeidae 0.30 0.013 Suspended POC (mg C m 2 ) n = 69 Total non calanoid copepods 0.32 0.007 Oncae idae 0.31 0.010 Miraciid ae 0.36 0.002 Fucoxanthin (g m 2 ) n = 69 Total non calanoid copepods 0.33 0.006 Oncaeidae 0.44 < 0.001 Sapphirinidae 0.31 0.009 Miraciid ae 0.46 < 0.001 Peridinin (g m 2 ) n = 69 Total non calanoid copepods 0.34 0.005 Oithonidae 0.25 0.036 Oncaeidae 0.28 0.022 Sapphirinidae 0.25 0.039 Particulate Organic Carbon (POC) Relationships between abundance of non calanoid copepods and larvacean s and particulate carbon concentrations measured as sediment trap flux at 200 m and in suspended form integrated through 200 m, were evaluated. Significant correlation between suspended POC and copepod abundance was found in the

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50 Figure 22 Cruise averaged individual larvacean abundance m 2 (0 200 m) for both large and small (< 2 mm and > 2 mm tail length) size categories at BATS (1995 1999 ). 0 2,000 4,000 6,000 8,000 10,000 12,000 14,000 11 Jan 16 Mar 27 Apr 12 Jun 22 Aug 10 Oct 16 Dec 14 Feb 15 Mar 9 Apr 7 May 10 Jul 3 Sep 5 Nov 13 Jan 7 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 13 Mar 8 Apr 3 Jun 11 Aug 22 Oct 8 Dec 29 Jan 24 Feb 8 Apr 1 Jun 3 Aug 12 Oct 9 Dec 1995 1996 1997 1998 1999 Copepods per square meter (0 200 m) < 2mm tail length > 2mm tail length

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51 case of total non calanoids and the families Oncaeidae and Miraciid ae. The strengths of the relationships were modest an d in the case of Miraciid ae negative (Table 7 ). The only significant correlation result found between POC from 200 m sediment traps and any of the taxa examined was for larvaceans. This seems reasonable as larvacean houses are a major source of marine snow in the ocean ( Alldredge, 1979). Role of non calanoid copepods in C and N dynamics at BATS Results of both Carbon Demand ( CD ) and Dissolved Inorganic Nitrogen Excretion ( DINE ) followed similar annual and seasonal patterns with an overall of 72 and 4.4 mg m 2 d 1 for C and N, respectively compared to an overall Primary Production (PP) of 463 mg C m 2 d 2 during the same time period Combined, non calanoid copepods made up an overall of ~ 28% (the slight difference between CD and DINE % result of differing effect of temperature) of all mesozooplankton CD and DINE at BATS, with slightly more than 1/3 contributed by Oithona spp ., 1/3 by Oncaea spp and ~ 1/4 by Corycaeidae. Thus, these three groups of copepods made up more than 90% of all non calanoid elemen tal dynamics. Highest seasonal estimates were found in spring (97 and 5.9 mg m 2 d 1 ) followed by summer (70 and 4.3 mg m 2 d 1 ) for CD and DINE, respectively. This was due to a combination of two important factors, animal abundance and water temperature. Spring had highest abundance of zooplankton while summer had slightly lower numbers but higher upper 200 m water temperatures. Lowest approximations for CD and DINE were recorded in fall and winter. Fall had slightly greater calculated CD and DINE than win ter (61 vs. 58 and 3.8 vs. 3.5 mg m 2 d 1 for CD and DINE, respectively). However, results from these 2 seasons were much closer compared to either spring or summer. Interestingly, the percentages of these seasonal estimates made up by non calanoid copepo ds (total and major groups) varied considerably among seasons as well as years examined much more so than in absolute terms. Total non calanoid absolute contribution to CD and DINE was highest in spring followed by summer (see Table 8 and 9 ) and lowest in winter with fall in between winter and summer in terms of absolute values. However, non calanoid copepods made up the highest percentage of mesozooplankton CD and DINE in summer and fall (~ 33 and 28%, respectively) closely followed by spring (~ 27%) and with winter having the lowest proportion of zooplankton carbon demand and nitrogen excretion made up by non

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52 calanoid copepods of all seasons (23%). Greater differences were found when individual groups of non calanoid copepods were examined. For example, O ncaea spp. had lowest CD and DINE (magnitude and %) in fall instead of winter while Corycaeidae had similar values for spring summer and fall with winter constituting less than half of in terms of both magnitudes and percentages. Table 8 Seasonal, annual and overall carbon demand (CD) of bulk mesozooplankton as well as total non calanoids, including the top 3 most abundant genera and families at BATS. Along with the percentage contribution of the various categories of non calanoid copepods to overall mesoz ooplankton estimates Bulk zooplankton C demand (mg C m 2 d 1 ) Carbon demand of non calanoid copepods (% of total mesozooplankton C demand) Total non calanoids Oithona spp. Oncaea spp. Corycaeidae Winter 58 13 (22.5%) 5.2 (9.0%) 4.6 (7.9%) 2 (3.5%) Spring 97 25.8 (26.6%) 8.8 (9.1%) 8.7 (9.0%) 6.8 (7.0%) Summer 70 22.9 (32.6%) 7.7 (11.0%) 6.6 (9.4%) 7.2 (10.2%) Fall 61 16.9 (27.7%) 5.8 (9.5%) 4.1 (6.8%) 5.3 (8.6%) 1995 55 21.7 (39.5%) 8.2 (15.0%) 7.1 (13.0%) 5.2 (9.1%) 1996 68 15.2 (22.3%) 5.0 (7.4%) 4.8 (7.1%) 4.1 (6.0%) 1997 68 17.3 (25.4%) 6.7 (9.9%) 4.4 (6.5%) 4.8 (7.1%) 1998 90 19.4 (21.5%) 6.3 (6.9%) 6.8 (7.6%) 4.9 (5.5%) 1999 76 25.3 (33.3%) 8.7 (11.5%) 7.7 (10.2%) 6.9 (9.1%) Grand average 72 19.8 (27.5%) 7.0 (9.7%) 6.2 (8.6%) 5.2 (7.2%) In terms of annual differences, highest calculated CD and DINE for bulk zooplankton were observed in 1998 (90 and 5.5 mg m 2 d 1 and lowest in 1995 (55 and 3.4 mg m 2 d 1 ) for CD and DINE, respectively. The years1996, 1997 and 1999 were closer to each other with respective values of (68, 68 and 76 mg C m 2 d 1 ) and (4.2, 4.1 and 4.6 mg N m 2 d 1 ). When viewed as a percentage of bulk zooplankton CD and DINE, non calanoid copepods made up highest proportions in 1995 (~ 4 0%) followed by 1999 (~ 34%) and 1997 (~ 26%). While 1998 and 1996 were years with lowest percentages mesozooplankton CD and DINE made up of non calanoid copepods (~ 22 and 23%, respectively). However, as was the case of seasonal averages, the absolute mag nitude of CD and DINE was not reflected in the proportions of these elements calculated for bulk zooplankton. The greatest quantity of C and N cycled through non calanoid copepods occurred in 1999 followed by 1995 and 1998 with respective values of (25, 22 and 20 mg C m 2 d 1 ) and (1.6, 1.4 and 1.2 mg N m 2 d 1 ) and lowest values were observed for 1996 and 1997 with an average

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53 Table 9 Seasonal, annual and overall Dissolved Inorganic Nitrogen Excretion (DINE) of bulk mesozooplankton as well as total non calanoids, including the top three most abundant genera and families at BATS. Along with the percentage contribution of the various categories of non calanoid copepods to overall mesozooplankton estimates Bulk zooplankton N excretion (mg N m 2 d 1 ) Nitrogen excretion of non calanoid copepods (% of total mesozooplankton N excretion) Total non calanoids Oithona spp. Oncaea spp. Corycaeidae Winter 3.52 0.82 (23.3%) 0.33 (9.4%) 0.29 (8.2%) 0.13 (3.7%) Spring 5.86 1.63 (27.8%) 0.56 (9.5%) 0.55 (9.4%) 0.43 (7.3%) Summer 4.27 1.45 (34.0%) 0.49 (11.5%) 0.41 (9.9%) 0.45 (10.5%) Fall 3.75 1.07 (28.5%) 0.37 (9.8%) 0.26 (7.0%) 0.33 (8.9%) 1995 3.36 1.37 (40.8%) 0.52 (15.5%) 0.45 (13.5%) 0.33 (9.7%) 1996 4.15 0.96 (23.1%) 0.32 (7.6%) 0.31 (7.4%) 0.26 (6.1%) 1997 4.13 1.09 (26.4%) 0.43 (10.3%) 0.28 (6.8%) 0.30 (7.3%) 1998 5.46 1.22 (22.3%) 0.40 (7.3%) 0.43 (7.9%) 0.31 (5.7%) 1999 4.62 1.60 (34.6%) 0.55 (12.0%) 0.49 (10.7%) 0.44 (9.4%) Grand average 4.37 1.25 (28.6%) 0.44 (10.1%) 0.39 (9.0%) 0.33 (7.5%) of (15 and 17mg C m 2 d 1 ) and (0.96 and 1.1mg N m 2 d 1 ), respectively. The annual pattern of the individual groups and genera followed that of total non calanoid copepods with only minor deviations. Thus, it appears that non calanoid copepods CD and DINE follow seasonal as well as annual patterns in terms of actual quantities of C and N cycled in the euphotic zone. However, they are much more variable seasonally and annually when viewed as a proportion of tota l mesozooplankton CD and DINE at BATS. Having calculated the amount of DIN excreted by bulk mesozooplankton as well as non calanoid copepods, it was a straight forward exercise to estimate th e amount of PP supported by zooplankton N excretion at BATS (Tab le 10 ). On the whole, mesozooplankton were able to support 6.3% of PP through excretion of DIN in the upper 200 m of the water column with non calanoid copepods composing 28% of this total. Oithona spp ., Oncaeid and Corycaeid copepods each made up 35, 32 and 26%, respectively, of the total non calanoid support of PP. Seasonal and interannual patterns of the amount of PP supported by zooplankton DIN regeneration in euphotic zone were influenced by 2 factors; 1) th e configuration of actual DIN of bulk mesozooplankton and non calanoid copepods (discussed above) and 2) the patterns of PP. The interplay between these 2 parameters led to a slightly different arrangement than that found for zooplankton elemental dynamics For example, DINE of zooplankton and PP were both highest in spring (5.9 and 542 mg m 2 d 1 for DINE and PP, respectively). However, when nitrogen cycling of bulk mesozooplankton was

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54 at its lowest level in winter (3.5 mg N m 2 d 1 ) PP was on par with sum mer (459 and 462 mg C m 2 d 1 respectively). Table 10 Percentage of primary production nitrogen demand met by non calanoid copepods and bulk zooplankton nitrogen excretion at BATS Primary production (N demand) mg m 2 d 1 Bulk zooplankton % Total non calanoids % Oithona spp. % Oncaeidae % Corycaeidae % Winter 459 (70) 5.16 1.18 0.48 0.42 0.19 Spring 542 (82) 7.14 1.98 0.68 0.67 0.52 Summer 462 (70) 6.33 2.07 0.70 0.60 0.64 Fall 371(56) 6.79 1.91 0.65 0.47 0.59 1995 468 (71) 4.86 1.94 0.74 0.64 0.46 1996 588 (89) 4.77 1.08 0.36 0.34 0.29 1997 430 (65) 6.34 1.68 0.65 0.43 0.46 1998 354 (54) 10.18 2.28 0.74 0.81 0.58 1999 463 (70) 6.82 2.28 0.79 0.70 0.62 Grand average 463 (70) 6.32 1.78 0.63 0.56 0.46 Additionally, when PP was at its lowest level in fall (371 mg C m 2 d 1 ) DINE of zooplankton was at moderate levels (3.8 mg C m 2 d 1 ). Results from a previous study by Dam et al., (1995) conducted in the spring at the BATS station found an average of 16 % of PP could be supported by mesozooplankton excretion of DINE in the euphotic zone. This higher percentage was due to 2 factors, namely lower springtime PP (339 mg C m 2 d 1 ) as well as much higher DINE (7.3 mg N m 2 d 1 ) in the photic layer due to signi ficantly increased mesozooplankton biomass in the Dam et al., study. Substantial differences were detected among the years examined in terms of the amount of PP based on regenerated DIN from zooplankton at BATS. For example, 1996 had the highest average PP among all the years examined (1995 1999) and was 2/3 higher than the lowest average found (1998); this led to the highest percentage support of PP by zooplankton excretion in 1998 and lowest in 1996 (see Table 9 ). The remaining years were relatively sim ilar in their average PP and the differences in the proportion of PP supported by recycled DIN were mainly due to differences in mesozooplankton abundance. The seasonal and annual trends for the support of PP contributed by non calanoids, including the mai n genera and families followed the same pattern as in DINE discussed above but with the additional factor of varying PP ( Table 10 ).

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55 The overall level of PP supported by recycled DIN within the euphotic zone calculated in this study was similar to that fo und by Al Mutairi and Landry (2001). They estimated an overall of 9.1% of total PP was supplied by mesozooplankton recycling of DINE in the euphotic zone at the HOT site. This was mainly due to higher mesozooplankton biomass at HOT than to either temperatu re or PP differences. Feeding strategies of Oithona spp. and their ecological significance to the BATS area M ost studies have shown that Oithona spp prefer motile prey including hetero and autotrophic flagellates including dinoflagellates, oligotrichines and cilliates (Lampit, 1978; Uchima and Hirano, 1986; Atkinson, 1995; Nakamura and Turner, 1997; Castellani et al., 2008) and do not consume diatoms even when these are abundant (Uchima, 1988) This may be a reason why the accessory photosynthetic pigment peridinin (representing dinoflagellates) was significantly correlated with Oithona spp abundance. Species of Oithona do not create a feeding cur rent as most calanoid copepods ( Paffenhfer, 1993) detected their prey by mechani cal and hydrodynamic perception and are ambush feeders that remain motionless in the water until they perceive either a motile cell or sinking particle (Svensen and Kirboe, 2000; Paffenhfer, 1998) Calanoid copepods and other crustacean zooplankton are known to produce compact and fast sinking fecal pellets (Paffenhfer and Knowles, 1979; Small et al., 1983). However, very few of them (~ 1 5% of production) are collected in sediment traps set below the euphotic zone (Bathmann et al., 1987; Turner, 2002). Reasons for this include bacterial degradation, disruption due to turbulence, and ingestion by other zooplanters (Karl et al., 1988; Alldredge and Silver, 1988; Turner, 2002). Coprophagy in Oithona spp. has been used to explain the ubiquity of the genus and the retention of fecal pellets in the upper layers of the ocean (Gonzlez et al., 1994; Gonzlez and Smetacek, 1994; Svensen and Nejstgaard, 2003). Gonzlez and Smetacek (1994) put forth the idea of Oithona spp. flux out of surface waters, especially when present in high numbers reaching 20 30% of daily carbon requirements. This could amount to an overall quantity of between 1.4 and 2.1 mg C m 2 d 1 of fecal pellets consumed by Oithona spp at BATS (from Table 7 ). Finally, as shown in a field study by Maar et al (2006) Oithona is negatively affected by turbulence (dissipation r ate of 10 7 to 10 6 m 2 s 3 ). L aboratory

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56 experiments have confirmed that clearance rates of ambush feeding copepods decrease with increasing turbulence likely by negating the advantage of highly sensitive setae in detecting potential food particles (Kirboe and Saiz, 1995; Saiz et al., 2003). It is speculated here that the increased vertical mixing and concomitant amplified turbulence may be one of the reasons for the winter minimum in Oithona spp abundance seen at BATS. Overall, Oithona spp was found to be the most numerous non calanoid genus at BATS and as such was established as the top non calanoid genus in terms of estimated carbon demand and regenerated nitrogen. Ecological role of the association of Oncaeidae with larvacean houses It was determined that abandoned larvacean houses produced in the euphotic zone at BATS could support the carbon demands of all Oncaeidae present in all seasons and years. Overall, estimated house C produced at BATS was 37 (new) and 95 (discarded) mg m 2 d 1 and Oncaeidae were capable of removing 17 6.6% of the carbon contained in newly produced and discarded houses, respectively (Table 11 ) This, of course, would be an upper bound since it would assume that 100% of the oncaeid diet comes from appendicul arian houses. When all other non calanoid carbon demand is included and assuming an exclusive diet of houses it was found to be capable of removing 54 to 21% of new and abandoned house carbon, respectively. Thus, larvacean houses can be an important food s ource for mesozooplankton at BATS. Seasonally, sp ring was the time of maximal CD for Oncaeidae as well as total non calanoid copepods due to high abundance; however, larvacean production was greatest during summer and fall due, in part, to higher temperatures in the upper 100m of the water column. This led to the highest proportion of house C utilization in spring amounting to 28 and 84% (new houses) to 11 and 30% (discarded houses) for Oncaeidae and total non calanoid ingestion, respectively (Tabl e 11 ) Following spring, summer was second in importance in terms of C D of both Oncaeidae and total non calanoids. The percentage of house C consumed in summer amounted to 14 and 48% of new (47 mg m 2 d 1 ) to 5 and 19% of the of discarded house C productio n (122 mg m 2 d 1 ) for Oncaeidae and total non calanoids, respectively. However, this

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57 Table 1 1 Seasonal, annual and overall results of larvacean house carbon production as well as total non calanoid, Oncaeidae and Corycaeidae rates of house consumption at BATS Larvacean House production (mg C m 2 d 1 ) Copepod carbon demand (mg C m 2 d 1 ) New houses Discarded houses Total non calanoids Oncaea spp. Corycaeidae (% of new house C % discarded house C) Winter 33.8 87.2 13.0 (38.5 14.9%) 4.6 (13.6 5.3%) 2 (5.9 2.3%) Spring 30.9 79.7 25.8 (83.5 29.6%) 8.7 (28.2 10.9%) 6.8 (22.0 8.5%) Summer 47.3 122.0 22.9 (48.4 18.8%) 6.6 (14.0 5.4%) 7.2 (15.2 5.9%) Fall 37.0 95.5 16.9 (45.7 17.7%) 4.1 (11.1 4.3%) 5.3 (14.3 5.6%) 1995 51.1 132.0 21.7 (42.5 16.4%) 7.1 (13.9 5.4%) 5.2 (10.2 3.9%) 1996 36.8 94.9 15.2 (41.3 16.0%) 4.8 (13.0 5.1%) 4.1 (11.1 4.3%) 1997 25.4 65.7 17.3 (68.1 26.3%) 4.4 (17.3 6.7%) 4.8 (18.9 7.3%) 1998 26.2 67.5 19.4 (74.1 28.7%) 6.8 (26.0 10.0%) 4.9 (18.7 7.3%) 1999 45.2 116.6 25.3 (56.0 21.7%) 7.7 (17.0 6.6%) 6.9 (15.3 5.9%) Grand average 36.6 94.5 19.8 (54.1 21.0%) 6.2 (16.9 6.6%) 5.2 (14.2 5.5%) was markedly lower than springtime due to significantly greater house production caused by higher larvacean abundance and upper 100 m water temperatures. Winter was a time of high larvacean abundance, second only to summertime numbers; however, house production was lower than either summer or fall mainly due to lower environmental temperatures (34 and 87 mg m 2 d 1 for new and abandoned houses, respectively). Fall on the other hand had the lowest larvacean abundance but due to higher water temperature s house production was the second highest of all seasons averaging a respective 37 and 96 mg m 2 d 1 for new and abandoned houses. Fall C demand of Oncaeidae and total non calanoid copepods amounted to a corresponding 4 and 18% of discarded house C to 11 and 46% of new house C produced. An important parameter affecting appendicularian house production was environmental temperature. Larvaceans were most abundant in winter and summer (3,600 and 3,670 m 2 respectively) and least during spring and fall (3,180 and 2,910 m 2 respectively) but house production was highest in summer and fall due in part to higher average temperatures in upper 100m of the water column (24.2 C for summer, 23.2 C for fall and 20.4 C for both winter and spring). Annually, larvace an house production was highest in 1995 and 1999 and lowest in 1997 and 1998 (Table 11 ). This could be attributed to the depth of wintertime mixing and the input of NO 3 into the euphotic zone leading to higher primary production and standing crops of autot rophs and heterotrophs,

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58 including metazoans (Steinberg et al., 2001). The C D related to standing crops, of Oncaeidae and total non calanoid copepod s did not exactly follow the patterns of larvacean house production and led to maximum percentage of house C consumption in 1997 and 1998 and lowest in 1995 and 1996 with intermediate values for 1999. Discussion Comparison to previous studies near BATS Several investigations on zooplankton biomass and community structure have been conducted in the vicinity of the BATS site over the past decades. They include Moore (1949), Menzel and Ryther (1961), Grice and Hart (1962) Deevey (1971), Deevey and Brooks (1 971), Deevey and Brooks (1977) and Bttger (1982). However, the studies of Deevey (1971) and Deevey and Brooks (1971, 1977) were the The Deevey (1971) s amples were collected biweekly from March 16 1961 to April 7 1962 using a 1 meter net of 203 m mesh, towed obliquely through the upper 500 m of the water column. Results of Deevey (1971) were used to compare annual and seasonal trends for the most impor tant genera and species of non calanoid copepods found at BATS. This was possible due to the use of the same mesh size to sample the zooplankton as the present study. Abundance data were averaged according to the month the tows were taken in both Deevey (1 971) and the present study. All abundance estimates (m 3 ) abundance per m 2 (0 200 m). The resulting composite monthly data showed total non calanoid numb ers to be in relatively good agreement, given the high variability of the data, in terms of seasonal pattern as well as absolute numbers found between the 2 studies (Figure 23a). In addition to total non calanoids, abundance data for five genera ( Oithona Corycaeus Farranula Oncaea and Mormonilla ) were also compared. The species examined included 5 Oncaea 2 Corycaeus and 2 Farranula species. When the agreem calanoid abundance, not a surprising

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59 result given the many different taxa that make up this category of copepods. For example Oithona spp. were found to be higher in abundance in the Deevey stu dy as compared to the present investigation for most of the composite months examined. The Deevey seasonally averaged abundance data for Oithona spp were well above those of the present for all seasons except summer. In addition, it was observed that tota l abundance of the genus Corycaeus was consistently below that found in the present study for all composite months. This trend was also reflected in seasonal comparisons. When the species C. flaccus and C. speciosus were compared it was found that both were generally higher in abundance in the Deevey study than in the present investigation, with maximum differences found in the composite month of November. Deevey (1971) mentioned that C. speciosus and C. flaccus were 1 st and 2 nd in terms of species abund ance among the 10 identified species. However, the present investigation found that they were 7 th and 5 th respectively while the top 2 Corycaeus species were C. typicus and C. limbatus The genus Farranula was not compared as a whole since its 2 constitu ent species had nearly opposite seasonal patterns. F. rostrata was nearly always more abundant in the present study than Deevey (1971) and averaged > 50% for all composite months combined. This contrasted with F. gracilis that was found to be slightly more abundant in the Deevey study compared to the present one (overall 10% less). Nonetheless, the basic seasonal patterns for these 2 species were similar among both studies. Seasonally, Farranula gracilis abundances from the Deevey study were more similar those of the present study than F. rostra which were lower for winter and spring, which happen to encompass the months of maximal populations for this species. One reason for the difference between the two studies for F. rostrata may be due to the different depths sampled. F. rostrata is a sub surface dwelling copepod and the Deevey samples were collected in the upper 500m versus 200m for the present study and therefore much of the water sampled would naturally not contai n this species. This would lead to lower abundance estimates per cubic meter of water and hence, lower numbers m 2 One of the most important genera compared between studies was Oncaea (encompassing all the newly defined genera in the family Oncaidae) It was also the genus with the most species, five in all, in which abundance data was presented in the study of Deevey (1971) enabling a direct contrast to the data set of the present investigation. Results of the comparisons showed Deevey total Oncaea spp. t o have a slightly different seasonal pattern with lower numbers in winter and spring and higher abundance in summer and

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60 Figure 23 (a f) Comparison between monthly averaged individual abundance m 2 (0 200 m) of non calanoid copepod taxa of Deevey (1971) and BATS (1995 1999). 0 5,000 10,000 15,000 20,000 25,000 30,000 All non calanoids (BATS) All non calanoids (Deevey) 0 500 1,000 1,500 2,000 2,500 3,000 Corycaeus spp. (BATS) Corycaeus spp. (Deevey) 0 2,000 4,000 6,000 8,000 10,000 12,000 14,000 Oithona spp. (BATS) Oithona spp. (Deevey) 0 500 1,000 1,500 2,000 2,500 3,000 3,500 Farranula gracilis (BATS) Farranula gracilis (Deevey) 0 1,000 2,000 3,000 4,000 5,000 6,000 7,000 8,000 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Oncaea spp. (BATS) Oncaea spp. (Deevey) 0 500 1,000 1,500 2,000 2,500 3,000 3,500 4,000 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Farranula rostrata (BATS) Farranula rostrata (Deevey)

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61 fall. Seasonally averaged data showed that spring and fall had the greatest deviations among the two studies with Deevey spring Oncaea spp abundance below the spring and fall BATS averages respectively. When individu al species were examined the situation was much different. Oncaea media from the Deevey study was nearly an order of magnitude lower in overall abundance. The difference was most pronounced March through June; the time of greatest abundance of O. media at BATS. None of the seasonal averages of the Deevey study was even close to those of the BATS data. Also, it is worthwhile pointing out that only female O. media at BATS were included in the counts and that the smaller and very similar looking species O. sc ottodicarloi was also enumerated separately. Oncaea scottodicarloi was not mentioned as being present in the Deevey study and it is strongly suspected that it was lumped in with O. media Both of these factors would tend to exacerbate the difference betwee n the two studies. It was thought that the greater depth sampled in the Deevey study had a hand in creating the discrepancy in O. media abundance between the two studies. Causes of observed seasonal and annual patterns in community structure and abundanc e Non calanoid copepod abundances at BATS were found to be variable at many time scales, including annual and seasonal time frames as well as the between cruise (monthly) and inter cruise level (days to hours). This can best be illustrated by analyzing the coefficient of variation (c.v) of abundance results. For all samples analyzed total non calanoid numbers had a c.v of 57% (n = 131 tows). Individual = 0.58, 96 = 0.46, 97 = 0.45, 98=0.58 and 99 = 0.59) while the case of pooled seasonal data revealed winter as the season with highest variability (c.v = 71%) and spring as a time of lowest c.v (42%). Summer and fall were close behind spring in terms of patchiness with c.v of 50 and 43%, respectively. However, when t he data were analyzed for within cruise variation using only cruises from which 2 replicate samples were enumerated (n = 60 cruises) the c.v was noticeably less than overall, annual or seasonal groupings (average = 26%) indicating a greater amount of varia tion among cruises than within. Previously mentioned results revealed statistically significant differences among seasons for many of the non calanoid groups identified as well as cases of significant differences among years sampled, although far fewer cas es.

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62 There are many possible sources of error involved in the enumeration of mesozooplankton including, but not limited to, shipboard collection uncertainties (flowmeter and depth recorder inaccuracies), imprecision of laboratory analyses (sub sampling and counting errors) as well as natural variability in the myriad of environmental factors controlling both absolute abundance and spatial distribution of the animals comprising the zooplankton community at BATS. The c.v can be seen as an upper bound to the h uman error involved in the analysis. The remainder is the natural variability inherent in the zooplankton community. No effort was made to separate or individually quantify these errors. The general seasonal abundance pattern of the majority of non calano id species observed in the present study was that of lowest numbers in winter, especially January, followed by significantly higher numbers in spring, particularly June. Early summer (July) also had elevated numbers of most non calanoid taxa analyzed. This was followed by lower numbers in late summer and fall. Although the exact timing and magnitude of the above pattern differed slightly between years, the general trend held. The proximate cause of the seasonal trend for the non calanoid community was, as expected, increased phytoplankton abundance and production. And although there were few significant correlations between PP and most non calanoid taxa abundance (only Oncaeidae and larvaceans had significant corre lations, Table 7 ) The seasonal cycle of the phytoplankton near the BATS site has been previously examined. Most notable of these early studies were those of Menzel and Ryther (1959). These authors mum production in late winter early spring (February April). They also noted significant interannual variation (Menzel and Ryther, 1960). These early observations have been confirmed by many other subsequent studies, especially those reporting results of t he BATS time series data over the past decade (e.g. Michaels et al., 1994 and Steinberg, 2001). Thus, it is not surprising to see mesozooplankton abundance, including the non calanoids, increase following the increased phytoplankton production of late wint er and early spring. But it is the degree of vertical mixing with its introduction of nutrients into the depleted euphotic zone that is the ultimate controller of primary production and indirectly zooplankton abundance. Thus, physical features that drive t he turnover of the upper layers of the water column and disrupt the nutricline need to be understood if the biological features of the BATS site are to be grasped.

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63 The BATS station is located in a transition area (25 and 32 N) of the Sargasso Sea between relatively productive waters to the north, where subtropical mode water is formed and oligotrophic southern regions to the south where the euphotic zone is permanently stratified and lies above the subtropical mode water (Steinberg, 2001). Cold fronts pas sing through the BATS region with their sustained high winds during mid winter (February to early March) mix the upper 150 300m layer of the water column and disrupt the seasonal thermocline as well as the nutricline. The North Atlantic Oscillation (NAO), defined as the difference in sea level pressure between the Icelandic low and the Azores high, influences seasonal winter mixing at BATS by controlling the strength and direction of westerly winds moving North Atlantic winter storm tracks either to a more northerly (positive phase) or southerly direction (negative phase). Since 1996, the NAO has been more positive (Philips and Joyce, 2007) leading to generally more mild winter mixing at BATS. Thus, most of the data presented in this study came from a more positive phase of the NAO. In addition to the decadal scale influences of NAO, there are many other physical features that likely enhance variability in non calanoid copepod abundance. These include mesoscale eddies (cold and warm core rings and mode water eddies) fine scale eddies as well as hurricanes that may cause increases in abundance not connected to the seasonal cycle. These features have been shown to greatly influence production in the upper layers of the water column including zooplankton biomass and abundance as well as primary production and particle fluxes (Roman et al., 1982; Dam et al., 1995). In discussing the relationship of zooplankton biomass with primary production at BATS Madin et al., (2001) found that standing stocks peaked during so me spring blooms while other blooms did not result in the same level of response by the mesozooplankton. Moreover, some augmentations in biomass occurred a month after primary production peaks while at other times no clear relationship existed between the parameters. As shown by Conte et al., (2003) and Jiang et al., (2007) mesoscale eddies can greatly enhance biomass at a given time and these features can be missed by the current sampling schemes (i.e. zooplankton sampling may occur within a passing featur e but primary production may be sampled from another parcel of water passing through the area). In an attempt to discern the response of non calanoid copepod abundance to ephemeral physical forcing of the upper ocean at BATS, selected well documented mesos cale eddies and hurricane events were

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64 examined. In late November 1996 Conte et al., (2003) tracked from October 6 1996 to January 15 1997 the consequences to particulate matter fluxes (3200m) of a warm mesoscale feature that passed through the vicinity of the Bermuda Testbed Mooring (BTM). The eddy was characterized by anti cyclonic rotation down to about 200m with an isothermal low salinity layer to approximately 180m and intermittent mixing to the base with concomitant entrainment of nutrients that caused a phytoplankton bloom (dominated by diatoms and prymnesiophytes) as measured at the BATS site. Particulate fluxes, production as well as zooplankton biomass were all elevated in mid December 1996 as the eddy was located right above the BTM and BATS sites Results of the present study showed increased average total non calanoid abundance from the December 1996 cruise (13,400 copepods m 2 ) compared to the month before and after (5,550 and 4,700, respectively). This increase was most pronounced in Oithona sp p abundance that was over 3 times year period examined for the month of December. In a related study Jiang et al., (2007) using ADCP data to estimate 200m integrated zooplankton biomass between August 1996 and November 2000 at the BTM site confirmed the results of Conte et al., as 1998 to February 4 1999. The event was characterized as a c old cyclonic eddy. However, unlike the warm feature described by Conte et al., (2003) this eddy did not result in elevated chlorophyll or zooplankton biomass as measured at the BTM site. Result of Jiang et al. (2007) were confirmed by findings of the pres ent study that revealed abundance of non calanoid copepods to be average for the time of year. However, as the edge of the eddy passed both chlorophyll and zooplankton biomass increased substantially. This was confirmed by elevated non calanoid abundance i n the February 12 1999 core cruise (2 tows) that was over 5 times greater than January 1999 core and bloom cruise results (4 tows) and twice the abundance found in the February 1999 bloom cruise (2 tows). This was hypothesized as being either an edge effec t of the eddy, normal spring bloom conditions, or a combination of both. In addition to mesoscale eddies, tropical storms and hurricanes frequently impact the BATS area. Jiang et al., (2007) examined the effect of 3 hurricanes (Edouard, Hortense and Lili) on zooplankton biomass at the BTM site. All three storms passed through the area between August and October 1996 with the eye of Lili as close as 170km to the BTM site. However, none of these storms elicited a significant response of chlorophyll or zooplan kton biomass as measured by Jiang et al., (2007) or

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65 affected the non calanoid abundance found in the present study. Jiang et al., (2007) did note that hurricane Fabian passing within 100km of the BTM area caused significant changes in chlorophyll and zoopl ankton biomass. They found that chlorophyll increased in the upper water column following passage of Fabian while depth integrated (0 200 m) zooplankton biomass was significantly reduced but that zooplankton biomass extended deeper into the water column. T noted by Roman et al., It should be kept in mind that the ephemeral physical features described above were passing over the BA TS area, transporting a water parcel containing zooplankton that had time to respond to the increased primary production brought about by increased nutrient input due to physical disruption of the nutricline. Also, not all of these events led to increased productivity and zooplankton standing stocks. R ecent studies have also shown increased zooplankton biomass and abundance both overall and for specific taxa within mesoscale features in the vicinity of the BATS site ( Goldthwait et al., 2008; Eden et al., 20 09) Assumptions used in estimating consumption of larvacean houses by oncaeid copepods The calculations of larvacean house C production and the proportion consumed by non calanoids, particularly the family Oncaeidae depend on two main assumptions. The first is that the equations used to estimate house production are both accurate and appropriate for use at BATS. The second assumption is that appendicularian houses serve as the main food source of Oncaeid copepods. T he estimates of carbon produced by new houses can be viewed as a lower bound while th ose estimated for discarded houses as an upper limit of carbon produced by appendicularians at BATS. This would serve to help constrain the C produc ed via houses at BATS. The reason for including estimates of new house C production instead of limiting it to discarded houses only was due to the fact that Sato et al., (2003) used 30 m screened seawater with Chlorophyll a of 0.2 to 2.0 g l 1 in their incubations while the Ch lorophyll a at BATS was at the lower end of that used in their experiments. Hence, it is possible that more particles would be attached at higher food concentrations than at lower ones.

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66 T he three species used to calculate the rate of production and carbon contents of houses in Sato et al., 2003 are known to be widely distributed in warm oceanic waters similar to those at the BATS site (Fenaux et al., 1998). Moreover, reports of the main families and species present in the BATS region (Northern Sargasso Sea ) mentioned by a variety of sources include the species used in the house production equations of Sato et al., 2003. Morris (1975) reported the larvacean species Oikopleura longicauda Fritillaria pellicauda F. borealis and Stegosoma magna present at Stat during a 1 year study while in the more comprehensive zooplankton study of Deevey (1971) at condition) were Oikopleura lo ngicauda Fritillaria pellicauda F. formica and F. tenella In addition to the immediate area of the BATS site Alldredge (1972) observed 3 species of larvaceans in the Florida Current near the Bahamas; O. longicauda O. fusiformis and Megalocercus abyssor um And Hopcroft and Roff (1998) reported Appendicularia sicula Fritillaria borealis sargass i, F. haplostoma, Oikopleura longicauda and O. dioica (a neritic species) from Jamaican waters (shallow eutrophic and mesotrophic areas and an oceanic oligotrophic site). Hence, it seems safe to list O. longicauda as a main species present at the BATS site along with various species of the smaller Fritillaria genus. Therefore, it does not seem unreasonable to use rates of house production and biomass estimates of ne wly produced and discarded houses of the O. longicauda O. fusiformis and O. rufescens calculated in Sato et al., (2003) as a proxy for house production at BATS. Fritillaria formica digitata had nearly double the house production rate of the highest measured Oikopleura 2003), however, no data on carbon content of new and discarded houses were available and this precluded the use of this estimate in the present stud y. The second assumption used in estimating the percentage of larvacean C production of houses consumed by Oncaeidae is that this family derives its nutrition mainly from the house itself as well as the attached particles. Many studies have show n that, of the copepods associated with discarded larvacean houses, members of Oncaeidae dominate in terms of numbers and that many of the species of the family commonly found in samples from the BATS site were seen on and in abandoned houses. These included Oncaea m editerranea (Alldredge, 1972; Ohtsuka et al., 1993; Green and Dagg, 1996, Ohtsuka et al., 1996), O. venusta (Ohtsuka and Kobo, 1991; Ohtsuka et al., 1993; Ohtsuka et al., 1996), Triconia conifera (Ohtsuka et al., 1993; Ohtsuka et al., 1996, Steinberg et al ., 1994 and 1997), O. media (Ohtsuka et al.,

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67 1993; Ohtsuka et al., 1996), T minuta and T dentipes (Ohtsuka et al., 1996). All of the previous studies also recorded a number of late copepodite stages presumably of the same species as the observed adults. In addition, gut content analysis of several species associated with larvacean houses revealed them to contain recognizable parts of the house (Ohtsuka and Kobo, 1991 in Ohtsuka et al., 1993, Ohtsuka et al., 1996; Steinberg et al., 1994). In addition, spec ies of Oncaeidae have been observed feeding on food collecting filters and other parts of discarded larvacean houses (Alldredge, 1972; Ohtsuka et al., 1996; Steinberg et al., 1997 ) Oncaeidae seem to be suited for taking advantage of large organic particles in the water column due to the anatomy of their feeding appendages. The mouthparts of Oncaeidae are adapted to feeding on large detrital material, such as discarded larvacean houses. Oncaei dae have s tout chelae bearing maxillipeds that along with the first antennae are used to grasp and to cling on to large objects, while their maxillules and maxillae are reduced and used only to scrape surfaces (Huys and Boxshall, 1991). From the evidence presented above it seems reasonable that Oncaeidae are associated with, and derive a significant portion of their nutritional requirements from, the contents of abandoned larvacean houses. This leads to several important implications to the transformation, cycling and transport of POM at the BATS site. The vast proportion of research into particle degradation (both physical alteration and chemical remineralization) has focused on the role of bacteria (e.g. Davoll and Silver, 1986; Cho and Azam, 1988) and to a lesser degree, the role of nanoflagellates and ciliates. This is especially the case when attempting to explain the sharp decline in POM with depth (Martin et al., 1987). However, Karl et al. (1988) concluded from experiments that POM was a poor site fo r microbial metabolic activity and theorized that other mechanisms must be at work to account for the loss of POM as it sinks from the euphotic zone. These were mainly physical processes such as abiotic fragmentation and solubilization, but a possible role of zooplankton ingestion was also invoked. Few studies have attempted to quantify the role of zooplankton in the transformation of marine detritus. Steinberg et al., (1997) quantitatively assessed the role of copepods in the degradation of meso pelagic gi ant larvacean houses. The authors concluded that associated metazoans (mainly copepods) were capable of removing an average of 1% and a maximum of 8% of the estimated house C d 1 through respiration depending on the number of animals present. That removal rate was suggested to be on par with

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68 the magnitude of bacterial remineralization. Combustion of detrital carbon is not the only way metazoans can decompose POM; they can physically transform marine snow by mechanical breakup through the act of feeding, an d can contribute to mass loss via growth, reproduction and production of fecal pellets. Steinberg et al., 1997 estimated that, combined with respiration rates, an average of 6% and a maximum of 43% of the C content of giant larvacean house in their study s ite could be removed on a daily basis and these numbers are in agreement with those calculated in the present study for Oncaeidae at BATS. Sapphirina spp. associations with salps at BATS The genus Sapphirina is known to have a peculiar relationship with Thaliaceans. Many species of Sapphirina are known to be parasitic consumers of Salps as early developmental stages turning to predators as adults (Heron, 1973; Harbison in Diebel 1998). Harbison (1998) listed 9 confir med species of Sapphirina associated with various species of thaliacea. Most of the Sapphirina species are not host specific and will utilize many different thaliacean species while a few were more host specific. Of the Sapphirina species mentioned by Harb ison, seven were found at BATS. Copilia spp may also, given their close relationship to Sapphirina spp. (particularly the phylosome morphology of the males), be associates of Thaliacea, but such a relationship has not been confirmed by any study as far as the author knows. Again, these members of Poecilostomatoida show themselves to be more benthic in their lifestyle than would be thought given that they live in the pelagic environment. As previously mentioned, 1996 was the year of maximum Sapphirina abund ance. In fact, the two cruises in April (9 th and 23 rd ) had much higher abundances than any other cruise for all 71 analyzed (range from 2 to 8 times higher). And w hen 1996 was broken down to the species level it was revealed that the dominant Sapphirina me tallina (Figure 14) was not most abundant in 1996, rather it was fairly consistent through the years with a slight maximum in 1995. The main species making up the April 9 th Sapphirina community were S. angusta S. ovolanceolata gemma and S. darwini while during the later part of April (23 rd ) S. nigromaculata and S. angusta dominated. In addition to Sapphirina spp. being unusually high, Copilia spp. represented mainly by C. mediterranea was also very high. What was unusual was that the normally dominant species S. metallina was actually lower in abundance than usual during this Sapphirina bloom. The only difference

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69 between S. metallina and the other species is that it is considered to b e a lower epipelagic species with most of the population residing below the mixed layer while the other species are more abundant within the mixed layer (Chae and Nishida, 1995). Lopez et al. (2007), through laboratory experiments, demonstrated that Sapphirina angusta has very high fecundity compared to most other egg carrying copepods (e.g. Oncaeidae, Corycaeidea and Oithonidae). Carrying egg sacs makes females more prone to visual predators (Paffenhfer, 1993; Kirboe and Sabatini, 1994), however, t he fact that females only seem to leave their salp host to mate with a male already attached to the outside of the host (Heron, 1973) tends to negate the increased mortality allowing Sapphirina angusta females to have egg production and growth rates that a re in the upper range for all copepods, and would seem to be necessary given the very patchy nature of salp blooms (Lopez et al., 2007). In addition, these same authors speculated that Sapphirina spp do not feed on suspended particles in the water and ins tead rely on attachment to biogenic aggregates in this case to salp bodies. It is interesting to note that while several species were abundant, S. angusta was the dominant one from the April 9 th cruise (~ 400 copepods m 2 ) and was still abundant during t he April 23 rd cruise, although less than in April 9 th (~ 60 copepods m 2 ) Except for one individual found in a December 1995 sample no Sapphirina angusta was encountered outside of the April 1996 cruises. It is suggested that during at least the beginning of Apr il 1996 there was a salp bloom. This was confirmed, as salps were found in high abundance (> 18,000 to 7,500 salps m 2 mainly larval forms) during the April 9 th and 23 rd cruises, respectively. Summary and conclusions Evidence suggest that copepods, especially non calanoids, play an important role in the transformation of particulate organic matter in the ocean and may account for the rapid loss of POC and PON with depth as measured by sediment traps, and the BATS site is no exception to these processes. Non calanoid copepods are abundant and make up a substantial portion of the copepod community at BATS. They are important players in both particle degradation through association and feeding on large agg regates such as the relation of Oncaeidae copepods with discarded larvacean houses and miraciid

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70 harpacticoids dependence on Trichodesmium colonies for food and as a nursery as well as the apparent feeding specialization by Oithona spp on fecal pellets of larger zooplankt on. Although much work still needs to be done in order to understand the feeding behavior and the subsequent ecological role of other numerous genera such as Farranula to elemental budgets at BATS it is hypothesized that most of the Poecilostomatoid copep ods have a feeding style that likens them to the role that detritivorous insects have in the terrestrial realm. These metazoans may even rival bacteria when it comes to degradation of marine snow and fecal pellets within the epipelagic zone and could be an important mechanism in retaining elements within the upper ocean. What is sorely lacking in the BATS core zooplankton sampling scheme is any sort of depth resolution. This is especially important since sinking marine snow particles tend to slow down and accumulate at density discontinuity interfaces such as the pycnocline and it may be an area where the much of the population of Oncaeidae and other copepods that are associated with sinking aggregates of POC could be located. Hence, it is imperative that zooplankton collection be conducted with much finer depth resolution than the current 200 m integrated depth sampling at BATS. Moreover, much more experimental work needs to be conducted to better understand the feeding behavior, physiology and life histo ries, and by extension the ecological impacts, of individual groups, genera and species at BATS. For example, zooplankton taxa suspected of having a major role in aggregate degradation could be incubated with varying sizes of marine snow as well as experim ents with only ambient levels of phytoplankton and microzooplankton. This would give some certainty regarding their role in particle dynamics in the water column. Also, it may be possible to find a chemical biomarker of detritus that would resist breakdown in the guts of these copepods and that may even be incorporated into the tissues of the detritovore. This would truly be a breakthrough and allow for a much better understanding of trophodynamics as well as elemental budgets at BATS. Only when adequately armed with biological knowledge at the level of the individual zooplankter, can truly meaningful models of elemental cycling be formulated that will lead to better predictions of how the world oceans will react to anthropogenic perturbations of atmospheric CO 2 in the future.

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71 Chapter Three Harpacticoid Copepods of the Family Miraciid ae: The Ecological Consequences of their Association with Trichodesmium spp. to the BATS Region

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72 Introduction Relatively few harpacticoid copepods, represented by 17 species or approximately 0.5% of the known species, have successfully made the transition from a benthic to a pelagic mode of life (Huys and Bttger Schnack 1994). However, those that have can be impo rtant components of the zooplankton community (Bttger Schnack 1989 and Uye 2002). Most species of pelagic harpacticoids are relatively poor swimmers and are usually associated with suspended particles in the water column (Huys and Bttger Schnack 1994 and Uye 2002). Of the particle associations of harpacticoid copepods perhaps the most interesting is the association between the 4 species of the family Miraciid ae and the colonial Cyanobacteria Trichodesmium Trichodesmium is a filamentous marine non hete rocystous cyanobaterium with wide spread distribution in tropical and subtropical oceans, particularly in oligotrophic systems and western boundary currents such as the Gulf Stream and Kuroshio currents, that is capable of fixing N 2 gas into organic nitrog en (diazotrophy) a capability first demonstrated by Dugdale et al. (1961). It has been studied extensively in many oceans around the world including the Pacific (Letelier et al., 1996; Karl et al., 1997; Tenrio et al., 2004), Indian (Capone et al., 1998 ; Lugomella et al. 2002) and the Atlantic which has received the most attention (Dugdale et al., 1961; Carpenter and Romans, 1991; Capone et al., 1997, Orcutt et al., 2001; Montoya et al ., 2002; McClelland et al., 2003; Carpenter et al., 2004). In additio n, Trichodesmium has been investigated in other areas such as the Caribbean (Carpenter and Price, 1977), the Gulf of Mexico (Holl et al., 2007) and the Red Sea (Post et al., 2002). Abundance and therefore significance of Trichodesmium production is favored in highly stratified and nutrient depleted euphotic zones (Hood et al., 2004). The genus Trichodesmium is present in either solitary filaments known as trichomes which are usually made up of around 100 cells or as one of 2 colonial forms generally composed of 100 200 trichomes each thought to be essential for maintaining simultaneous C fixation with the evolution of O 2 and N 2 fixing enzymes (nitrogenase) that need low O 2 environments to function properly. These conditi ons are thought to arise through the interplay of mucilage and DON production by Trichodesmium supporting metabolic activities of a rich heterotrophic microbial community

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73 associated with the colonies providing microzones of low O 2 that facilitate N 2 fixati on (Paerl et al., 1989). The 2 colonial forms have been reported to maintain different vertical distributions in the Gulf of Aqaba in the Red Sea with > 95% of the tuft colonies restricted to the upper 50m and 62 81% of the puff forms found between 50 an d 100m of the water column (Post et al., 2002). However, this pattern remains to be verified in other ocean systems. One of the more peculiar behaviors of Trichodesmium is their reported ability to control their vertical distribution in the ocean through pressure resistant gas vacuoles (Walsby et al., 1978). Most Trichodesmium biomass is found in the upper euphotic zone between 10 and 50 m (Letelier et al., 1996; Orcutt et al., 2001; Carpenter et al., 2004). However, colonies as well as single trichomes are frequently found at deeper depths below the nutricline (Letelier et al., 1996; Orcutt et al., 2001). This has led to theories that Trichodesmium may indirectly contro d store phosphate (Karl et al., 1992). The theory basically states that by the time Trichodesmium become depleted in phosphate they have stored enough carbohydrates that acting as ballasting agents enabli ng them to sink below the nutricline and allowing the Cyanobacteria to collect and store phosphate. While in deep waters away from an adequate light source the stores of carbohydrates are utilized and along with the pressure resistant gas vacuoles cause th e trichomes and colonies to rise again to the upper euphotic zone to begin C and N fixation using the stores of phosphate. This was supported by evidence of differential C : N and N : P ratios of sinking and rising colonies in surface (5 m) and deep (100 m) water in the central Pacific gyre (Letelier and Karl, 1998). However, Trichodesmium colonies from an experimental isolate have been shown to be unable to recover after 3 6 days in the dark (White et al., 2006). Thus, there may be a time constraint on th e vertical migratory ability of colonies. A rich and diverse community of flora and fauna are associated with Trichodesmium colonies. These include herterotrophic bacteria (Paerl et al., 1989; Sheridan et al., 2002) as well as a host of different phytoplan kton including cells of prokaryotic species, diatoms, autotrophic dinoflagellates and chrysophytes as well as many protistan and metazoan species (Sellner, 1992; Sheridan et al., 2002). Sheridan et al. (2002) estimated associated organisms of Trichodesmiu m to be, on average, 2 5 orders of magnitude more enriched within colonies than surrounding seawater with colony morphology influencing the presence of, as well as, the variety associated organisms Puffs were more likely to contain associates and to have a

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74 greater number of species than tuft forms and it has been theorized that this form represents a successive stage of tuft form with more mucoid matrix. However, they did notice that harpacticoids were found more frequently on tufts colonies. Macrosetella gracilis and most likely all 4 species of Miraciid ae use Trichodesmium as a physical substrate and as a food source. Bjrnberg (1965) found that M. gracilis were intimately associated with Trichodesmium and were dependent on the Cyanobacteria for habitat as well as food. She also found significantly higher survival rates for nauplii of M. gracilis Oculosetella gracilis and Miracia efferata when Trichodesmium thiebautii trichomes were added. Calef and G rice (1966) found that Macrosetella gracilis was tightly coupled to Trichodesmium colony abundance in the western tropical Atlantic. In addition, O'Neil (1998) observed female M. gracilis physically attaching their eggs to Trichodesmium colonies. This help ed explain how the non swimming nauplii were able to attach to the floating Cyanobacteria. In addition, several studies have quantitatively demonstrated feeding on Trichodesmium in 3 of the 4 known miraciid species with the focus on M. gracilis (Roman, 197 All of the investigations on the ability of M. gracilis as well as other species of miraciid harpacticoids to ingest Trichodesmium and assimilate its carbon and nitrogen points to their importance as a dire ct link between Cyanobacterial production and higher trophic levels. This may be especially important quantify, in both absolute and relative terms, the amount of Trichodesmium C and N grazed and, in the case of N recycled at BATS.

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75 Materials and Methods Sample collection and p rocessing Samples analyzed for Miraciid abundance and ecology were gathered and analyzed as described in chapter 1. In addition to identification and enumeration total length, (with and without caudal rami) of all Miraciid copepods found in the samples, was measured using a micrometer to the ne arest 20m. Biomass e stimates The published metabolic equations used to calculate rates of grazing, excretion, and assimilation were expressed in terms of carbon biomass. Hence, good estimates of individual biomasses were imperative. Thus several indep endently derived estimates of carbon biomass were employed in this study. Two different published length carbon regression equations were used to estimate the carbon content of the Miraciid s in this study. The first by Satapoomin (1999) was of Macrosetell a gracilis gathered from the Andaman Sea off Phuket Island, Thailand. A total of 55 M. gracilis were measured and the results of individual length (in m) and carbon content (in g) were transformed to natural logs before calculating the following regressi on equation: L n C weight = 1.59 (SE 0.21) ln total length 10.92 (SE 1.44) with R 2 = 0.51. The second equation used to estimate Miraciid copepod biomass was the length dry weight relationship of Webber and Roff (1995) for what they termed Macrosetella sp p Copepod samples were collected from shallow waters (average depth 20 m) south of Kingston Jamaica over an 18 month time period. Measured dry weights (g) and lengths (m) were transformed to natural logs before running the regression analysis. The foll owing equation was the result for Macrosetella spp data: L n dry weight = 2.52 (SE 0.07) ln prosome length 16.03 (SE 0.52) with an R 2 of 0.97. For the present study dry weight was converted to carbon mass by assuming a carbon content of 50% of dry weig ht. In addition to length weight equations, overall average individual carbon biomass results from 3 ot her studies were used. Table 12 lists average individual carbon content as well as sampling location and study references.

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76 Table 12 Individual m iraciid copepod biomass estimates from previous studies Species Biomass(g C ind 1 ) Sampling location Reference Macrosetella gracilis 5.1 (SE 0.34) n = 35 Upper 50m of the Gulf Stream off of Miami Roman (1978) 7.2 (SE 0.19) Sep n = 10 3.8 (SE 0.28) Jan n = 24 Upper 30m Bahamas Upper 30m Eastern Caribbean 5.57 Upper 30m Bahamas to Eastern Caribbean Oculosetella gracilis 3.94 Miracia efferata 8.7 Roman (1994) Results of the two independently derived equations using the prosome length (without caudal rami) data from this study were very low when compared to the average results of 5.1 g C per individual (Roman, 1978). Roman (1978) also measured t he prosome length (range = 1.16 1.44 mm) and the results = 0.11). The results were improved when total length (including caudal rami) was used. Both types of measurements were used to estimate individual carbon content from the 2 weight length equations discussed above. For this study, a total of 8 estimates of carbon biomass were used for Macrosetella gracilis. Four were from published weight length regression equations and 4 from overall averages determined in other studies listed in Table 12 Oculosetella gracilis and Miracia efferata carbon biomasses were estimated by the 4 regression equations (2 different eq uations using prosome and total length as dependent variables) as Distioculus minor were determined from the regression equations only. Carbon specific grazing r ates For this study the quantity of Trichodesmium carbon and nitrogen ingested by Macrosetella gracilis was determined using a total of four grazing estimates from three published studies and one rate

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77 was used for each of Oculosetella gracilis and Miracia effer ata determined in one study. Distioculus minor grazing rates were estimated using the rate determined for Macrosetella gracilis (1994). All rates used in this study are listed in Table 13 along with the species and colony morphology of Trichodesmium used in the experiments. Grazing rates were determined by first averaging results of each specific ingestion equation using the various biomass estimates of individual species, then taking the mean of all the different grazing functions to o btain an overall average. It was this grand average that was utilized as the Trichodesmium ingestion rate estimate in this study. All grazing rate equations were for the amount of carbon consumed, therefore, to determine the quantity of nitrogen ingested a C : N ratio of 6.6 was applied to the results. Table 13 Pub lished grazing rates of miraciid copepods Species g C ingested g copepod C 1 d 1 n = replicates Temperature C Trichodesmium species and colony morphology Reference Macrosetella gracilis 1.08 (SE 0.09, n = 47) 22 T. thiebautii (puff) Roman (1978) 0.75 (SE 0.14, n = 18) 23 27 T. thiebautii (tuft) (1994) 0.41 (SE 0.72 n = 3) 29.5 (Sep) T. thiebautii (tuft) 2.69 (SE 1.32 n = 8) 25.7 (Jan Feb) Oculosetella gracilis 0.77 (SE 0.36, n = 3) 23 27 T. thiebautii (tuft) (1994) Miracia efferata 1.11 (SE 0.35, n = 8) 23 27 T. thiebautii (tuft) (1994) Nitrogen excretion r ates Excretion rates of miraciid copepods at BATS were estimated using results of the studies of Verity Microsetella rosea and Macrosetella gracilis collected by vertical to (1996) conducted isotopic 15 N experiments involving measurement of N ingestion and excretion as well as

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78 investigating the effects of certain parameters on NH 4 concentration. The results from both studi es are summarized in Table 14 Table 14 Published rates of nitrogen excretion for Macrosetella gracilis g N excreted g copepod C 1 d 1 n = replicates Temperature C Sampling location Reference 0.076 (n = 10); Non feeding ~ 27 Sargasso Sea Verity (1985) 0.089 (SE 0.03, n = 17); Non feeding 28 29 Upper 30 m Eastern Caribbean 0.360 (SE 0.07, n = 14); Feeding 28 29 Upper 30 m Eastern Caribbean The 3 resulting metabolic rates were used to calcu late nitrogen excretion of all miraciid copepods at BATS on a per m 2 basis. Rates were applied to all 4 species and used all biomass estimates, as was previously done for grazing rate equations. The results from each equation were then averaged to obtain an overall est imate of nitrogen excretion by miraciid copepods at BAT S. Assimilation and C p ortioning Assimilation of C by miraciid In her investigation C assimilation rates as well as the sequence of its incorporation among the various biochemical pools wit hin Macrosetella gracilis were calculated using 14 C labeled Trichodesmium thiebautii Results of the partitioning experiments revealed that, over a 24 hour period, incorporated 14 C was 0.31 g C g copepod C 1 d 1 (SE 0.05, n = 24) for September 1991 an d 0.48 g C. g copepod C 1 d 1 (SE 0.07, n = 24) for both January and February 1992. Assimilation of ingested C (expressed as % of ingestion) was determined by dividing the total amount of C incorporated by the quantity ingested (determined separately) An average of 76% of ingested

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79 C was assimilated for the September 1991 cruise while 22 and 15% was incorporated for January and February 1992, respectively. This gave an overall average of 21% calculated by averaging all 3 incorporation rates and divid ing by all 3 ingestion rates and 38% calculated by averaging the 3 incorporation percentages (i.e. 76, 22 and 15%). The latter was the percentage applied in the present study to estimate carbon assimilation by all miraciid copepod species at BATS. Trich odesmium C and N standing stock and production at BATS In order to fully investigate the ecological role of miraciid copepods at BATS, data on Trichodesmium colony abundance as well as C and N standing stocks and production were needed. The study of Orcutt et al. (2001) satisfied all of the above requirements. These authors conducted a seasonal study of Trichodesmium at Station BATS for the period of January 1995 to November 1997 except June and October of 1995 when samples were gathered at Hydrostati were collected on mon thly cruises f r o m 15 20 min surface drift tows using a 1 m 2 335m mesh net fitted with a General Oceanics flowmeter. Colonies of Trichodesmium were separated into the morphologically distinct for study. In addition to surface sampling, a series of tows were conducted at various depths (0, 20, 50, 75 and100m) during May, August and October 1995 and October 1995 in order to estimate vertical distribution of Trichodesmium colonies. Rates of Trichodesmium N fixation were determined for individual colonies by 15 N 2 isotopic uptake as well as the acetylene reduction method. However, only the 15 N 2 isotopic uptake results were used in this study since they were more extensive. Results of the 15 N 2 incorporation experiments revealed an overall average rate of colony N 2 fixation of between 0.03 .74 nmol colony 1 h 1 0.04 .80 nmol colony 1 h 1 f 2 fixation by colonies of Trichodesmium colonies at BATS on an annual basis was 0.001 mol N m 2 y 1 during1995, 0.005 mol N m 2 y 1 during1996 and 0.004 mol N m 2 y 1 during1997 for an overall average of 0.004 mol N m 2 y 1

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80 Carbon fixation by Trichodesmium at BATS was measured monthly using the 14 C bicarbonate incorporation technique. Individual colony rates of primary production had an overall average of 17.54 nmol C colony 1 h 1 (SD=11.08). For the present investigation results of integrated colony N 2 fixation m 2 (figure 10b, Orcutt et al., 2001) were used to compare Miraciid copepod grazing to organic nitrogen production of Trichodesmium. In addition, Trichodesmium nitrogen standing crop (g N m 2 ) was calculated by multiplying the mean monthly particulate nitrogen doubling times by the daily nitrogen fixation rates (figure 6, Orcutt et al., 2001). Trichodesmium carbon fixation rates were derived by multiplying the production C:N ratio by the daily rate of nitrogen fixation m 2 and carbon standing stocks m 2 were obtained by multiplying nitrogen standing stocks of all cruises by 6.6 the C:N of Trichodesmium at BATS (Karen Orcutt, personal communication) Statistical methods Relationships between miraciid copepod and Trichodesmium colony abundance at BATS were investigated by way of the Spearman Rank analysis (a non parametric anaolog of the Pearson product moment correlation coefficient). In addition, seasonal and annual abundance analysis was con ducted using the non parametric Kruskal Wallis test due to the violation of parametric test assumptions by the data (i.e. non normal distribution).

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81 Results Seasonal and interannual trends in miraciid a bundance Harpacticoid copepods of th e family Miraciid ae consist of four species, all of which were represented at BATS. The species were, in order of numerical importance, Macrosetella gracilis Oculosetella gracilis Miracia efferata and Distioculus minor Overall, members of this family co nstituted just 0.8% of total non calanoid abundance at BATS. However, this small number belies their ecological importance, as will be discussed in coming sections. The most important species of Miraciid ae was Macrosetella gracilis composing more than hal f (56.7%) of total abundance for this family followed by Oculosetella gracilis (21.7%), and Miracia efferata and Distioculus minor each composing approximately 11% of all miraciid abundance Annual differences were seen for the family as a whole with hig hest numbers in 1999 and 1997 (176 and 143 animals m 2 s.d = 148 and 139) and lowest in 1995 and 1998 (59 and 63 copepods m 2 s.d = 57 and 67) while 1996 was intermediate in abundance with 95 individuals m 2 (s.d = 137). When the data were analyzed usin g the non parametric test of Kruskal significant (K W, p = 0.003; Multiple Comparisons (M.C), p = 0.025). Seasonal analysis indicated very strong patterns with winter and fall always having higher abundance than ei ther spring or summer (K W, p < 0.001; all M.C p values < 0.001 except between winter and summer with p = 0.009). Overall means with standard deviation (s.d) of seasonal Miraciid populations were as follows: winter 163 (152), spring 51 (61), summer 61 (7 8) and fall 174 animals m 2 (137). The high variability within seasons was likely enhanced by annual differences although the seasonal patterns were always the same within years. In addition, it should be noted that the pattern of abundance was largely governed by the onset of the de ep winter mixing that normally began in late February and ceased in late April or early May after which began the physical setting preferred by Trichodesmium (i.e. stratified water column with a shallow nutrient depleted mixed layer) with a gradual build u p of Trichodesmium colonies th at were followed by increasing miraciid abundance. Peak abundances of both colonies and miraciid s were found in late summer through early winter (Sep Jan) or until the onset of the seasonal deep mixing events. Hence, winter wa s a season that

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82 presented both Trichodesmium and their associated Miraciid harpacticoids with very different environments one hospitable early on becoming hostile towards the end. Turning to individual species of Miraciid ae, Macrosetella gracilis had a si milar annual abundance pattern as did the family as a whole for the 5 years examined (1995 1999). This is not surprising given the numerical dominance of the species. However, there was some distinction in the strength of these differences. In the case of Macrosetella gracilis 1997 and 1999 were significantly greater than 1995 (K W, p = 0.003; M.C, p = 0.042 and 0.017 for 1997 and 1999, respectively). Figure 24 shows abundance data of M. gracilis for all years analyzed at BATS. Seasonally, M. gracilis show ed an identical configuration as the Miraciid ae as a whole, with winters and falls having significantly more copepods than springs or summers (K W, p < 0.001; M.C, all p values < 0.001 but between winter and summer where p = 0.011). The next most dominan t species was Oculosetella gracilis (Figure 24 ). This species was most abundant in 1997 and 1999 and least in 1995 and 1996 with significant differences between 1996 and both of 1997 and 1999 (K W, p = 0.002; M.C = 0.022 and 0.045 for 1997 and 1999, respec tively). The pattern of seasonal changes in population were similar to Macrosetella gracilis except that Oculosetella gracilis had its peak average abundance in winter only and lowest numbers were found in summer while spring and fall had very similar averages. With respect to statistical significance, differences were found between winter and both spring and summer 0.001; M.C, w inter spring, p = 0.002 and winter summer p < 0.001). The last two species of Miraciidae found at BATS, Miracia efferata and Distioculus minor had less distinct annual and seasonal arrangements (Figure 25). Annual differences, although not statistically significant, were suggested by the means. The pattern for Distioculus minor was similar to that exhibited by the Oculosetella gracilis with highest densities in 1997 and 1999 but slightly different in terms of minimum numbers which occurred in 1996 and 19 98 (rather than 1995). However, annual trends were not the same for Miracia efferata Highest numbers were seen in 1996 (instead of 1997) and 1999 while lowest abundance was found during 1997 (not 1995) and 1998. Seasonally, Miracia efferata had maximum n umbers in fall and lowest in spring (> order of magnitude difference; K W, p < 0.001) while summer and winter were intermediate in scale (nearly 50% of fall numbers). Distioculus minor exhibited highest populations in winter and fall and lowest in spring a nd summer with significant differences between

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83 Figure 24 Cruise averaged individual abundance m 2 (0 200 m) of Macrosetella gracilis and Oculosetella gracilis at BATS (1995 1999) 0 50 100 150 200 250 300 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Copepods per square meter (0 200 m) Macrosetella gracilis Oculosetella gracilis

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84 Figure 25 Cruise averaged individual abundance m 2 (0 200 m) of Miracia efferata and Distioculus minor at BATS (1995 1999) 0 20 40 60 80 100 120 140 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Copepods per square meter (0 200 m) Maracia efferata Distioculus minor

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85 winter and fall (K W, p = 0.013). All miraciid average annual and seasonal abundance data is presented in Appendix 4. Relationship between miraciid and Trichodesmium colony abundance In an attempt to analyze the ecological role of miraciid copepods at BATS one of the first aspects to be considered was the correlation between copepod and Trichod esmium colony abundance. If there was a close relationshi miraciid copepods depending on Trichodesmium colonies for food, shelter and as a nursery for their young as demonstrated in many previous studies (Bjrnberg, 1965; correlation between their respective abundances. The first step in examining the relation between the miraciid copepods and colonies of Trichodesmium at BATS was to plot cruis e averaged (1995 1997) abundance of both (Figure 2 6 ). In addition to total miraciid s, the cruise averaged abundance of all four constituent species was plotted along with Trichodesmium colony abundance (Figures 27 30 ). miraciid Macrosetella gracilis and Miracia efferata Trichodesmium colony abundance; however, it appeared that increases in miraciid species abundance lagged those of the colonies. Correlation s between miraciid copepod and Trichodesmium colony abundance at BATS were tested using Spearman Rank analysis. No significant correlations were found between abundance of total miraciid s or any of the four species and Trichodesmium colonies (Table 15 ). H owever, as suggested by the plots, when the data were lagged (i.e. Trichodesmium colony abundance from a cruise is paired with miraciid species abundance of the following one to four cruises) the results were dramatically different. Total miraciid copepods Macrosetella gracilis and Miracia efferata had significant correlations and R values that increased from a one month lag to peak at a 3 month lag (Table 15 ) decreasing after a four month lag in the case of total miraciid abundance and becoming non signif icant for M. gracilis and M. efferata This pattern suggests a minimum response time (egg to adult) of 4 8 weeks for miraciid copepods to increases in Trichodesmium colony abundance.

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86 Table 15 Results of Spearman Rank analysis of cruise averaged miraciid copepod species and Trichodesmium colony abundance m 2 (0 200 m) for the period 1995 1997 concomitant and lagged miraciid data Abundance m 2 No lag n = 36 1 month lag n = 34 2 month lag n = 34 3 month lag n = 33 4 month lag n = 32 Trichodesmium colony Total miraciid copepods R value p value n.s 0.34 0.048 0.47 0. 005 0.57 < 0.001 0.41 0.022 Macrosetella gracilis R value p value n.s 0.50 0.002 0.60 < 0.001 0.63 < 0.001 n.s Oculosetella gracilis R value p value n.s n.s n.s n.s n.s Miracia efferata R value p value n.s 0.50 0.002 0.58 < 0.001 0.60 < 0.001 n.s Distioculus minor R value p value n.s n.s n.s n.s n.s *n.s ( results not significant ) Miraciid copepod grazing of Trichodesmium at BATS The overall estimate of Trichodesmium C and N grazed by all species of miraciid copepods at BATS for the entire 5 year study period (1995 1999) was 372 and 56 g m 2 d 1 for C and N, respectively. The overall seasonal con figuration was for higher fall and winter grazing (due to higher miraciid abundance) and lower spring and summer rates. Annual variability in grazing followed population abundances of the constituent Miraciid copepod species. Tables 16 and 17 list annualiz ed and seasonal daily ingestion rates per m 2 for individual populations as well as all 4 species combined for C and N, respectively. Highest grazing rates occurred during 1997 and 1999 more than twice that found in the years 1995 and 1998. Seasonal differ ences in grazing rate were greater than those found interannually, with winter and fall generally more than a factor of 5 greater than spring and nearly a factor of 3 higher than summer. However, when there were some deviations from the general seasonal p attern. The first deviation was in 1995 when, starting from a low ingestion rate of 108 g C and 16 g N m 2 d 1 for winter and a slight decline in spring (79 g C and 12 g N m 2 d 1 ) daily grazing rates jumped three fold to 306 g C and

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87 Figure 26 Cruise averaged individual abundance m 2 (0 200 m) of miraciid copepods and Trichodesmium colonies (from Orcutt et al., 2001) at BATS (1995 1997) 0 200 400 600 800 1000 1200 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Abundance per square meter (0 200 m) Total Miraciid copepods Trichodesmium spp. Colonies

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88 Figure 27 Cruise averaged individual abundance m 2 (0 200 m) of Macrosetella gracilis and Trichodesmium colonies (from Orcutt et al., 2001) at BATS ( 1995 199 7) 0 200 400 600 800 1000 1200 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Abundance per square meter (0 200 m) Macrosetella gracilis Trichodesmium spp. Colonies

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89 Figure 2 8 Cruise averaged individual abundance m 2 (0 200 m) of Miracia efferata and Trichodesmium colonies (from Orcutt et al., 2001) at BATS (1995 1997). 0 200 400 600 800 1000 1200 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Abundamce per square meter (0 200 m) Maracia efferata Trichodesmium spp. Colonies

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90 Figure 29 Cruise averaged individual abundance m 2 (0 200 m) of Oculosetella gracilis and Trichodesmium colonies (from Orcutt et al., 2001) at BATS (1995 1997). 0 200 400 600 800 1000 1200 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Abundance per square meter (0 200 m) Oculosetella gracilis Trichodesmium spp. Colonies

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91 Figure 30 Cruise averaged individual abundance m 2 (0 200 m) of Distioculus minor and Trichodesmium colonies (from Orcutt et al., 2001) at BATS (1995 1997). 0 200 400 600 800 1000 1200 11 Jan 14 Feb 16 Mar 11 Apr 11 May 12 Jun 11 Jul 22 Aug 12 Sep 10 Oct 6 Nov 16 Dec 30 Jan 14 Feb 15 Mar 9 Apr 7 May 10 Jun 10 Jul 5 Aug 3 Sep 8 Oct 5 Nov 14 Dec 13 Jan 7 Feb 4 Mar 8 Apr 5 May 11 Jun 15 Jul 11 Aug 12 Sep 6 Oct 14 Nov 9 Dec 1995 1996 1997 Abundance per square meter (0 200 m) Distioculus minor Trichodesmium spp. Colonies

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92 Table 16 Annual and seasonal Trichodesmium carbon grazed by miraciid copepods at BATS from 1995 to 1999 Miraciid species Season g C ingested m 2 d 1 (s.d) 1995 n = 25 1996 n = 24 1997 n = 30 1998 n = 25 1999 n = 27 Macrosetella gracilis Winter 69.3 (56.8) 111.1 (136.2) 546.9 (424.7) 233.8 (214.7) 781.4 (442.6) Spring 54.5 (62.0) 45.1 (85.9) 139.6 (191.5) 21.5 (39.8) 133.0 (153.1) Summer 199.0 (251.5) 106.5 (130.6) 98.6 (162.1) 197.0 (344.0) 283.2 (447.9) Fall 107.8 (75.0) 927.8 (323.0) 524.7 (410.1) 199.9 (136.5) 697.4 (473.6) Annual 104.4 (138.9) 292.1 (415.2) 371.3 (390.4) 152.1 (212.5) 478.4 (465.2) Oculosetella gracilis Winter 30.2 (32.7) 12.7 (18.0) 111.9 (74.0) 41.2 (58.2) 99.5 (20.4) Spring 16.2 (19.7) 6.9 (15.8) 35.9 (29.8) 33.9 (43.6) 35.0 (48.0) Summer 15.5 (19.7) 6.0 (14.6) 8.0 (9.3) 7.6 (18.6) 21.3 (33.7) Fall 23.2 (34.5) 46.0 (57.9) 16.8 (18.1) 19.6 (22.5) 51.1 (39.4) Annual 20.8 (26.5) 17.4 (34.4) 56.9 (66.9) 25.9 (39.1) 32.1 (36.7) Miracia efferata Winter 4.5 (11.1) 0.0 (0.0) 10.1 (15.9) 13.9 (34.1) 145.2 (145.1) Spring 0.0 (0.0) 0.0 (0.0) 24.8 (39.2) 0.0 (0.0) 11.4 (32.2) Summer 85.1 (208.6) 16.2 (25.9) 19.3 (35.2) 24.7 (30.6) 90.6 (96.9) Fall 78.1 (89.3) 211.7 (200.5) 43.5 (80.2) 46.4 (51.3) 40.7 (80.6) Annual 37.1 (109.9) 57.0 (131.4) 21.5 (42.9) 20.4 (35.9) 72.2 (108.2) Distioculus minor Winter 3.6 (6.2) 0.0 (0.0) 18.3 (17.11) 5.9 (9.28) 18.8 (24.3) Spring 7.9 (7.4) 2.7 (4.6) 5.0 (8.8) 2.2 (3.9) 0.9 (2.5) Summer 6.6 (7.9) 3.2 (5.5) 0.0 (0.0) 1.2 (2.9) 3.9 (8.6) Fall 8.0 (13.4) 5.6 (5.3) 1.8 (4.5) 12.2 (11.5) 28.0 (37.6) Annual 6.6 (8.4) 3.1 (4.7) 8.3 (14.0) 5.2 (8.4) 12.8 (23.8) All species Winter 107.7 123.8 687.1 295.0 1044.9 Spring 78.6 54.7 205.3 57.6 180.3 Summer 306.2 131.9 125.8 230.5 398.9 Fall 217.1 1191.1 585.0 278.0 817.3 Annual 169.0 369.6 458.1 203.7 595.4

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93 46 g N m 2 d 1 in summer with fall showing a slight decline to 217 g C and 33 g N m 2 d 1 In addition, 1997 had nearly double the ingestion rate for spring compared to summer. The likely reason for this was the very deep and prolonged winter mixing event of 1995 and the shallow and brief winter mixing period in 1997 (Hood et al., 2001) Both years were extreme v alues of the entir e 5 year data set (see figure 31 especially 0 100 m integrated water temperatures). Macrosetella gracilis becomes evident. It constituted just over 77% of overall C and N grazing at BATS for the period of 1995 to 1999, and dominated seasonally as well The average percentage of overall Miraciid C and N ingestion contributed by M. gracilis were 62, 79, 81, 75 and 80% corresponding to 1995, 1996, 1997, 1998 and 1999. In addition, Macrosetella gracilis contributed 77, 69, 74 and 80% of overall Miraciid C and N grazing for winter, spring, summer and fall, respectively. The second most importa nt species, in terms of grazing pressure on Trichodesmium colonies, was Miracia efferata Although lower in overall abundance than Oculosetella gracilis it was, nonetheless, much larger in body mass (8.7 vs. 3.9 g C ind 1 ). The percentage of total miracii d copepod grazing made up by this species was 11% for both C and N ingestion. This was closely followed by Oculosetella gracilis that contributed of 9.7% of Trichodesmium consumption at BATS while the smallest member of the family Miraciid ae, Distioculus m inor composed only 2% of total miraciid grazing. Table 17 Annual and seasonal Trichodesmium nitrogen ingested by miraciid copepods at BATS from 1995 to 1999 Miraciid species Season g N ingested m 2 d 1 (s.d) 1995 n = 25 1996 n = 24 1997 n = 30 1998 n = 25 1999 n = 27 Macrosetella gracilis Winter 10.5 (8.64) 16.86 (20.71) 83.14 (64.57) 35.57 (32.64) 118.79 (67.29) Spring 8.29 (9.43) 6.86 (13.07) 21.21 (29.14) 3.29 (6.07) 20.21 (23.29) Summer 30.21 (38.21) 16.21 (19.86) 15.00 (24.64) 29.93 (52.29) 43.07 (68.07) Fall 16.36 (11.43) 141.00 (49.07) 79.71 (62.36) 30.36 (20.71) 106.00 (72.00) Annual 15.86 (21.14) 44.36 (63.07) 56.43 (59.36) 23.14 (32.29) 72.71 (70.71) Oculosetella gracilis Winter 4.57 (5.00) 1.93 (2.71) 17.00 (11.21) 6.29 (8.86) 15.14 (3.07)

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94 Table 17 (continued) Miraciid species Season g N ingested m 2 d 1 (s.d) 1995 n = 25 1996 n = 24 1997 n = 30 1998 n = 25 1999 n = 27 Spring 2.43 (3.00) 1.07 (2.43) 5.43 (4.50) 5.14 (6.64) 5.29 (7.29) Summer 2.36 (3.00) 0.93 (2.21) 1.21 (1.43) 1.14 (2.79) 3.21 (5.14) Fall 3.50 (5.21) 7.00 (8.79) 2.57 (2.71) 3.00 (3.43) 7.79 (6.00) Annual 3.14 (4.00) 2.64 (5.21) 8.64 (10.14) 3.93 (5.93) 4.86 (5.57) Miracia efferata Winter 0.71 (1.71) 0.00 (0.00) 1.57 (2.43) 2.14 (5.21) 22.07 (22.07) Spring 0.00 (0.00) 0.00 (0.00) 3.79 (5.93) 0.00 (0.00 ) 1.71 (4.93) Summer 12.93 (31.71) 2.43 (3.93) 2.93 (5.36) 3.79 (4.64) 13.79 (14.71) Fall 11.86 (13.57) 32.14 (30.50) 6.57 (12.21) 7.07 (7.79) 6.21 (12.21) Annual 5.64 (16.71) 8.64 (20.00) 3.29 (6.50) 3.07 (5.43) 11.00 (16.43) Distioculus minor Winter 0.57 (0.93) 0.00 (0.00) 2.79 (2.57) 0.93 (1.43) 2.86 (3.71) Spring 1.21 (1.14) 0.43 (0.71) 0.79 (1.36) 0.36 (0.57) 0.14 (0.36) Summer 1.00 (1.21) 0.50 (0.86) 0.00 (0.00) 0.21 (0.43) 0.57 (1.29) Fall 1.21 (2.07) 0.86 (0.79) 0.29 (0.71) 1.86 (1.71) 4.29 (5.71) Annual 1.00 (1.29) 0.50 (0.71) 1.29 (2.14) 0.79 (1.29) 1.93 (3.64) All species Winter 16.36 18.79 104.43 44.86 158.79 Spring 11.93 8.29 31.21 8.79 27.43 Summer 46.57 20.07 19.14 35.00 60.64 Fall 33.00 181.00 88.93 42.29 124.21 Annual 25.64 56.14 69.64 30.93 90.50 Seasonally, the portion of Trichodesmium ingestion by each species varied, with Oculosetella gracilis exhibiting a higher contribution in winter and spring (13.4 and 22%) and lower value s ( 5% ) for both summer and fall. The pattern for Miracia efferata was the exact opposite of O. gracilis with the greatest portion of miraciid grazing in summer and fall (20 and 13%) and lowest percentage in winter and spring (7 and 6%). These seasonal patterns may be related to differing temperature preferences of the 2

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95 species. The last species of miraciid copepod, Distioculus minor had no clear seasonal pattern in terms of contribu tion to total Trichodesmium grazing at BATS but it was slightly higher in winter and fall (2.2 and 3.3%) compared to summer and spring (1.3 and 1.8%). Trichodesmium C and N standing crop consumed In order to better understand the ecological impact of miraciid copepod grazing at BATS, the proportion of Trichodesmium standing crop, in terms of C and N, consumed by miraciid s was evaluated. Over the 3 year period (1995 1997) that data was collected on Trichodesmium colony abundance as well as C and N fixat ion rates (Orcutt et al., 2001), it is estimated that, as a group, miraciid copepods consumed some 12.3% each of colony C and N standing crop Interannually, p roportio nal ingestion rates were 3.9, 8.3 and 24.7% for 1995, 1996 and 1997, respectively, for b oth C and N standing crop. Seasonally the pattern was for highest overall proportions of standing C and N crops to be grazed during spring (25.9%) and lowest in summer (0.8%), while intermediate values were found for both winter and fall (15.2 and 11.3%, r espectively). Table 18 Percentage of Trichodesmium carbon standing crop consumed by miraciid copepod species at BATS for the period 1995 1997 Species Macrosetella gracilis Oculosetella gracilis Miracia efferata Distioculus minor All species % Trichodesmium C standing crop consumed Annual 1995 2.4% 0.5% 0.9% 0.14% 3.9% 1996 6.8% 0.7% 0.7% 0.05% 8.3% 1997 18.3% 3.3% 2.5% 0.51% 24.7% All years 9.2% 1.5% 1.4% 0.23% 12.3% Seasonal Winter 11.7% 2.7% 0.4% 0.40% 15.2% Spring 17.7% 3.4% 3.2% 0.58% 24.9% Summer 0.5% 0.04% 0.2% 0.02% 0.8% Fall 8.7% 0.7% 1.8% 0.06% 11.3%

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96 As discussed in the previous section on miraciid copepod grazing, the bulk of all Trichodesmium colonies consumed at BATS (1995 1997) by miraciid s were by Macrosetella gracilis (74.6% of C an d N standing crop ). The annual and seasonal trends in these proportions for each of the 4 species followed the same patterns discussed in previous sections. Details of the contrib ution each Miraciid species made to the daily depth integrated removal of Trichodesmium C and N standing crop at BATS for the period of 1995 to 1997 are listed in Tables 18 and 19 respectively. Table 19 Percentage of Trichodesmium nitrogen standing crop consumed by miraciid copepod species at BATS for the period 1995 1997 Species Macrosetella gracilis Oculosetella gracilis Miracia efferata Distioculus minor All species % Trichodesmium N standing crop consumed (g N m 2 d 1 ) Annual 1995 2.43% 0.57% 0.86% 0.14% 3.93% 1996 6.86% 0.71% 0.71% 0.05% 8.36% 1997 18.43% 3.36% 2.50% 0.51% 25.00% All years 9.21% 1.57% 1.36% 0.23% 12.36% Seasonal Winter 11.71% 2.71% 0.43% 0.40% 15.21% Spring 17.79% 3.43% 3.21% 0.59% 25.00% Summer 0.57% 0.07% 0.14% 0.02% 0.79% Fall 8.71% 0.64% 1.79% 0.06% 11.29% Nitrogen e xcretion by miraciid c opepods Miraciid grazing of Trichodesmium could also be a source of excreted nitrogen, derived from fixed N 2 gas, available as NH 3 to other phytoplankton at BATS. To this end the N excretion of miraciid cop epods was calculated (Table 20 ). This resulted in an overall average of 27 (57 including feeding excretion rate) g N m 2 d 1 as ammonia by all species of Miraciid ae at BATS for all years analyzed (1995 1999). Macrosetella gracilis contributed just over 71% of this total and Oculosetella gracilis Miracia

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97 efferata and Distioculus minor each contributed 14.5, 11.3 and 3.0%, respectively. Annual and seasonal t rends of nitrogen excretion at BATS followed those of grazing discussed above. Comparing overall mean rates of miraciid copepod N excretion with that of ingestion, it was noticed that excretion was on par with estimated Trichodesmium grazing rates (57 vs 56 g N m 2 d 1 ). This discrepancy was improved by 47% when only N excretion rates of non feeding animals were included in calculating miraciid release of inorganic nitrogen and amounted to 27 vs. 56 g N m 2 d 1 for N grazing Table 20 Trichodesmium nit rogen excreted by miraciid copepods at BA TS for the period of1995 to 1999 Miraciid species Season g N excreted m 2 d 1 (s.d) 1995 1996 1997 1998 1999 Macrosetella gracilis Winter 9.8 (8.1) 15.8 (19.3 ) 77.6 (60.3) 33.2 (30.5) 110.9 (62.8) Spring 7.7 (8.8) 6.4 (12.2) 19.8 (27.2) 3.0 (5.7) 18.9 (21.7) Summer 28.2 (35.7) 14.6 (18.3) 14.0 (23.0) 28.0 (48.8) 40.2 (63.6) Fall 15.3 (10.6) 131.7 (45.8) 74.5 (58.2) 28.4 (19.4) 99.0 (67.2) Annual 14.8 (19.7) 41.3 (59.0) 52.7 (55.4) 21.6 (30.2) 67.9 (66.0) Oculosetella gracilis Winter 6.9 (7.4) 2.9 (4.1) 25.5 (16.8) 9.4 (13.2) 22.6 (4.6) Spring 3.7 (4.5) 1.6 (3.6) 8.2 (6.8) 7.7 (9.9) 8.0 (10.9) Summer 3.5 (4.5) 1.4 (3.3) 1.8 (2.1) 1.7 (4.2) 4.8 (7.7) Fall 5.3 (7.8) 10.5 (13.2) 3.8 (4.1) 4.5 (5.1) 11.6 (9.0) Annual 4.7 (6.0) 4.0 (7.8) 12.9 (15.2) 5.9 (8.9 ) 7.3 (8.3) Miracia efferata Winter 0.7 (1.8) 0.0 (0.0) 1.6 (2.5) 2.2 (5.4) 22.9 (22.8) Spring 0.0 (0.0) 0.0 (0.0) 3.9 (6.2) 0.0 (0.0) 1.8 (5.1) Summer 13.4 (32.8) 2.5 (4.1) 3.0 (5.5) 3.9 (4.8) 14.3 (15.3) Fall 10.7 (14.0) 33.3 (31.6) 6.8 (12.6) 7.3 (8.1) 6.4 (12.7) Annual 5.5 (17.2) 9.0 (20.7) 3.4 (6.8) 3.2 (5.7) 11.4 (17.0) Distioculus minor Winter 0.8 (1.4) 0.0 (0.0) 4.2 (3.9) 1.4 (2.1) 4.3 (5.5) Spring 1.8 (1.7) 0.6 (1.0) 1.1 (2.0) 0.5 (0.9) 0.2 (0.6)

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98 Table 20 (continued) Miraciid species Season g N excreted m 2 d 1 (s.d) 1995 1996 1997 1998 1999 Summer 1.5 (1.8) 0.7 (1.3) 0.0 (0.0) 0.3 (0.7) 0.9 (2.0) Fall 1.8 (3.1) 1.3 (1.2) 0.4 (1.0) 2.8 (2.6) 6.4 (8.6) Annual 1.5 (1.9) 0.7 (1.1) 1.9 (3.2) 1.2 (1.9) 2.9 (5.4) All species Winter 18.3 18.7 108.8 46.1 160.7 Spring 13.2 8.6 33.0 11.3 28.8 Summer 46.7 19.3 18.8 33.8 60.2 Fall 33.1 176.7 85.1 42.9 123.4 Annual 26.5 55.0 70.9 31.9 89.5 Assuming a C : N of 6.6 for bulk phytoplankton at BATS the overall amount of depth integrated primary production supported by Trichodesmium nitrogen, recycled by miraciid copepods, was just under 0.1%, and ranged from This number, although very low, should be seen in the context that the source is fixed N 2 gas and that this new production is quickly made available to other phytoplankton speci es, including species that are not toxic and are a food source for other zooplankton. As with all rates discussed so far, annual and seasonal trends of total Miraciid s and individual species tracked that of grazing rates. Table 2 1 lists the percentage of p rimary production measured at BATS (0 140) supported by Trichodesmium N released by way of miraciid copepods for all years and seasons. Briefly, total miraciid N excretion support of primary production was highest in 1997 and 1999 (0.13 and 0.15%) and lowe st in 1995 and 1998 (0.05 and 0.07%) and seasonally, the highest proportions were found in winter and fall (0.14 and 0.15%) and lowest in spring and summer (0.03 and 0.06%).

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99 Table 21 Percentage of pr imary production (Integrated to 140 m and assuming a C : N of 6.6) supported by miraciid copepod N excretion at BATS (1995 1999) Species Macrosetella gracilis Oculosetella gracilis Miracia efferata Distioculus minor All species Annual 1995 0.026% 0.008% 0.010% 0.002% 0.046% 1996 0.052% 0.005% 0.010% 0.001% 0.069% 1997 0.096% 0.025% 0.006% 0.004% 0.131% 1998 0.044% 0.011% 0.007% 0.003% 0.065% 1999 0.111% 0.019% 0.016% 0.005% 0.151% Seasonal Winter 0.097% 0.027% 0.008% 0.004% 0.136% Spring 0.015% 0.009% 0.001% 0.001% 0.027% Summer 0.039% 0.004% 0.012% 0.001% 0.056% Fall 0.117% 0.012% 0.021% 0.005% 0.154% Discussion Validity of assumptions used The present study of the role of miraciid copepods in the transfer of C and N to higher trophic levels at BATS is predicated on 2 key assumptions that must hold up in order for the results to be valid. The first, and most important, supposition is that Trichodesmium forms a major if not total p ortion of the diet of miraciid harpacticoids and the second assumption is that Cyanobacteria production is made available to other zoo plankton through predation of miraciid s Support for the first assumption comes from several sources. The first line of evidence pertains to the similar global distribution of Trichodesmium and miraciid copepods, particularly M. gracilis For example, Calef and Grice (1966) found a strong correlation in the Atlantic between M. gracilis abundance and that of Trichodesmium co lonies (0 200m) in the vicinity of the north east portion of South America while similar findings were found more recently by Bttger Schnack (1989) in the Red Sea. By itself, presence of Trichodesmium colonies and miraciid copepods in

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100 the same area is cir cumstantial and does not constitute evidence of feeding on the Trichodesmium tissue itself or even close connection to their colonies. Actual associations of M. gracilis with Trichodesmium were observed more than half a century ago when Krishnaswamy (19 49) observed nauplii and copepodites of this species to be physically attached to filaments within colonies of the Cyanobacteria. T he author suggested that some of the unique features of M. gracilis morphology hooked antennae and mandibles were an adaptati on to clinging to filaments of Trichodesmium I n a later study by Bjrnberg (1965) it was noted that nauplii of the 3 species of Miraciid ae examined ( M. gracilis Miracia efferata and Oculosetella gracilis ) that did not attach themselves to Trichodesmium filaments not only failed to dev elop properly but eventually died In addition to laboratory observations, several authors have observed Miraciid nauplii attached to Trichodesmium colonies in the field in different ocean systems (Bjrnberg, 1965; Tokioka and Bieri, 1966; Borstad, 1978; Ohki and Fujita, 1982; Ohki et al., 1992). Thus, evidence exists for an obligate association between Trichodesmium and, at least naupliar stages of, Miraciid copepods. In addition to nauplii, copepodites and adults of M. gr acilis also posses hooked appendages (maxillae and maxillipeds) that allow them to tightly grasp filaments of Trichodesmium and they were also and R M. gracilis was observed in the act of feed ing on filaments of Trichodesmium However, there are opposing points of view regarding the nutritional importance of Trichodesmium to mira ciid copepods. A study by Nair et al (1980) speculated, but did not offer concrete evidence, that miraciid copepods do not derive nutrition from the Trichodesmium but rather from other phytoplankton associated with greater overall production from input o f nutrients by the Cyanobacteria colonies. While another study (Borstad and Borstad, 1977) hypothesized that miraciid nauplii did not feed on Trichodesmium itself but rather on the associated community of fauna and flora. Nevertheless, the associated heter otrophic bacteria and protozoa likely derive a substantial portion of their nutrition from of DOC and DON exuded from the Trichodesmium itself (Paerl et al., 1989; Sellner, 1992). A recent study, Eberl and Carpenter (2007) analyzing stable isotope ratio 15 N and 13 C) of epipelagic copepods, as well as the gut contents of adult M. gracilis in the north Pacific central

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101 gyre near Hawaii concluded that M. gracilis did not derive a significant amount of its ration from feeding on Trichodesmi um due to 15 N of M. gracilis M. efferata and calanoids (3.1, 1.80 and Trichodesmium cells in any M. gracilis guts examined. The authors also found no statistically significant correlation between M. gracilis and Trichodesmium abundance in contrast to findings of Calef and Grice (1966). However, there are some issues with the methods and conclusions of Eberl an d Carpenter. Firstly, the authors of the study correlated trichome rather than colony abundance an important point as it is the colonial form of Trichodesmium that Miraciid s associate with and not individual free trichomes. Secondly, Eberl and Carpenter ( 2007) stated that most gut material of adult M. gracilis analyzed could not be identified and only 1 animal out of 18 examined had a remnant of a diatom ( Rhizosolenia sp With 2 cells of Richelia Cyanobacterium inside) while most (n = 6) gut contents coul d not be identified (10 had completely empty gut).The authors admitted that their results did not disprove per se that M. gracilis feeds on Trichodesmium and that the copepod could have ingested Trichodesmium cell contents and not the cell wall a conclusio n supported by observation of the feeding behavior of M. gracilis that has been observed to consume Trichodesmium However, Eberl and Carpenter stated that their isotope data did not support this possibility. An early study in the Pacific ( Wada and Hattori 1976) of Trichodesmium 15 N reported a signature of only 2.0 In contrast, zooplankton from deeper depths with no Trichodesmium were much more enriched 15 in the heavy nitrogen isotope In a more recent study, Montoya et al., 2002 15 N in zooplankton from areas of Trichodesmium blooms in North Atlantic becoming lower Gulf of Mexico at offshore stations for bulk zooplankton in the smaller size classes of 250 15 N 1.6 to 2 .2 13 C enrichment of 19. 7 to18.2 1000 m size categories ratios indicative of substantial incorporation of Trichodesmium organic matter into higher trophic levels Holl et al., 2007 13 C for Trichodesmium and bulk POC to av erage 13.86 ( 11 to 15) and 25.00 ( 27 to 22) 15 N signatures measured by Eberl and Carpenter (2007) actually lie within the

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102 expect ed enrichment of 1 trophic transfer from Trichodesmium to primary consumer Hence it is likely that 15 N rather than the miraciid s being enriched. Other studies using the newer method of analyzing stable isotopic an alysis of amino acids, specifically those with high turnover (citric acid cycle intermediaries) in copepods such as glutamic acid and those with low turnover (i.e. structural components) such as phenylalanine, have shown a significant amount of N incorpora tion into the smaller size fractions (250 500 m) of zooplankton originated from Trichodesmium (McClelland et al., 2003). In addition to plausible explanations for the isotopic results of Eberl and Carpenter (2007), several previous studies have quantitat ively shown through experiments that miraciid copepods (specifically, M. gracilis O. gracilis and M. efferata ) actually consume and even assimilate C and N into their tissues ). For example, il and Roman (1994) examined the potential of several species of copepod s to feed on Trichodesmium in order to identify grazers of the Cyanobacterial colonies and of all the species of copepods examined only the miraciid harpacticoids ingest ed and assimila te d Trichodesmium carbon. 1998 ) demonstrated that M. gracilis not only consumes Trichodesmium but also incorporated its C into copepod tissue with an estimated assimilation rate of 38 %. Moreover, and very importantly to the Miraciid feeding assumption used in the M. gracilis did not feed on whole water C 14 labeled phytoplankton ( ). Finally, ingestion and regeneration of Trichodesmium N by M. gracilis was verified by O'Neil et al. (1996) using 15 N 2 labeled colonies E xcretion of M. gracilis may be an important way in which newly Trichodesmium N can be made available to rest of the autotrophic community. Thus, while there are some who raise the possibility that miraciid copepods may not derive all their nutritional needs from Trichodesmium the vast majority of evidence points to the confirmation of Trichodesmium as a main food source for these copepods The assumption that miraciid copepods are consumed by other zooplankton predators and thus transfer Trichodesmium production of organic C and N to higher trophic levels is supported by less evidence. However, there is no proof against this due to either toxicity of the miraciid copepods or to the inability o f other predators to consume them while attached to Trichodesmium colonies. Borstad and

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103 Brinckmann Voss (1979) described the athecate hydroid Pelagiana trichodesmiae common on Puff colonies only, as a voracious predator of nauplii and adult copepods of M. gracilis However, the only ion by larger zooplankton on a miraciid copepod species is that of Post et al., 2002 who analyzed long chain polyunsaturated essential fatty acids of zooplankton. These lipids are rarely synthesized in metazoans and thus reflect the diet of the animal consumers (St John and Lund, 1996). In addition, phytoplankton have a conservative composition of polyunsaturated fatty acids that makes it possible t o pinpoint the autotrophic food source of secondary consumers (Brett and Mller Trichodesmium and found large amounts of it in M. gracilis of their chaetognath samples and concluded that they must have fed on M. gracilis as the only other zooplankter containing the Trichodesmium lipid b iomarker was Salpa maxima and these were much too large to be consumed by the chaetognaths. Finally, Post et al., 2002 rejected the possibility that the Trichodesmium degradation and subsequent pass age through the microbial loop since no calanoids contained the lipid and the amounts contained in M. gracilis were qui et high. The preponderance of the evidence points to M. gracilis a nd likely all other species of miraciid copepods deriving much of, if n ot all, their nutritional needs from Trichodesmium and perhaps the associated heterotrophic bacterial community. In addition, there are other pathways an d means of trophic transfer by miraciid copepods. One is sloppy feeding that likely plays a role in the transfer of DOC and DON to higher trophic levels by way of the microbial loop. Another is through excretion of DIN and DON resulting in enhanced general phytoplankton production through increased uptake of the regenerated N fixed by Trichodesmium All of these processes mediated by m iraciid copepods (i.e. grazing, secondary production and trophic transfer, sloppy feeding and enhanced N regeneration) are important to the ecology, oceans, particularly in oligotrophic regions and especially during blooms of Trichodesmium.

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104 Role of Trichodesmium and their gr azers in C and N budgets at BATS Conditions conducive to formation and maintenance of Trichodesmium blooms include highly stratified and low nutrient waters with low standing stocks of phytoplankton with the overall result of high light levels that seem to be a prerequisite for Trichodesmium success (Hood et al., 2002) Maximum Trichodesmium abundance an d by extension Trichodesmium C and N production at BATS is found during late summer and early fall when waters are most stratified and nutrient depleted, and are at their lowest during late winter and early spring when deep mixing occurs and other phytopl ankton species are at their peak standing crops (Orcutt et al., 2001). Trichodesmium bloom formation is driven by light availability and seed populations remaining in the stratified portion of euphotic zone following winter/spring mixing (Hood et al., 2001 ). The factor of seed population is important to bloom formation due to the low growth rate of Trichodesmium with doubling times of about 3 6 days (Capone et al., 1997). Thus, interannual variation in Trichodesmium colony (1995 1997) and m iraciid copepod a bundance (1995 1999) are inversely related to the depth and duration of the late winter and early spring vertical mixing events at BATS. Years of maximal phytoplankton production (e.g. 1995) are also years of lowest m iraciid and Trichodesmium standing crop s and production. In addition, summer storms can also affect Trichodesmium abundance. For example 3 hurricanes passed through the BATS area in August and September 1995 further preventing the summer and fall build up in Trichodesmium biomass that was refle cted in low m iraciid abundance during this time period as well as during early winter of 1996 (see Figu re 31 ). Hood et al. (2001) demonstrated that the general pattern of Trichodesmium abundance is roughly correlated to the North Atlantic Oscillation (NAO) with the negative phase related to increased amounts of Trichodesmium shift to a negative phase in 1995. However, since 1996, the NAO has been more positive (Philips and Joyce, 2007) leading to generally more mild winter mixing at BATS and this is reflected in the data of Trichodesmium (1996 and 1997) and m iraciid abundance (1996 1999).

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105 A likely reason for the above pattern is due to a time delay between miraciid copepod and Trichodesmium colony population changes with miraciid numbers generally lagging behin d those of the colonies For example, although Trichodesmium colony abundance is high in early summer (July) to mid fall ( November) miraciid populations do not begin to increase until late summer (September) and remain high up to early winter (January) suggesting that colony increases occur faster than the miraciid population c an respond (a time lag of approximately 6 weeks) Finally, r esults of the present study suggest that in addition to microbial utilization and degradation of Trichodesmium colonies a significant portion of the standing crop may be consumed by miraciid copepods. Using results of Orcutt et al. (2001) an overall (1995 1997) average of just over 12% of Trichodesmium standing crop of both C and N was consumed by miraciid copepods with a minimum in 1995 of slightly less than 4% and a maximum in 1997 of nearly 25%. The majority (75%) of the grazing was by Macrosetella gracilis alone with the remainder almost equally split between Oculosetella gracilis and Miracia efferata Distioculus minor had a trivial (< 2%) contribution to Trichodesmium C and N co nsumption at BATS mainly due to their low abundance and small body size Summary and conclusions Trichodesmium plays a key role in upper ocean food webs and nutrient dynamics they have been hypothesized to be driving some systems to P limitation and may ultimately have a hand in global climate regulation. Trichodesmium likely enhances total pelagic productivity i ncluding both non diazotrophic primary productivity and the microbial loop especially during the very stratified nutrient depleted conditions favored by this autotroph through DON and DOC produced through exudation and cell lysis. However, it appears that Trichodesmium is not readily grazed upon by metazoans due to physical and mechanical reasons, poor nutritional quality, or toxins produced by the Cyanobacteria. The most common species T. thiebautii is well known to produce a type of neurotoxin. However, t he harpacticoid copepods of the family Miraciidae have been established as active consumers of all Trichodesmium species including the highly toxic T. thiebautii The great importance of Trichodesmium to global oligotrophic tropical and

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106 subtropical pelagic systems coupled with the lack of direct metazoan grazers makes species of Miraciidae particularly important as conduits of diazotroph productivity to the general zooplankton community. However, much remains to be rigorously established. Questions that nee d to be answered include the following: 1) Do other species of zooplankton graze on the non toxic species of Trichodesmium such as T. erythraeum ? 2) Do miraciids consume other phytoplankton or marine snow? 3) Do miraciids consume Trichodesmium in the free trichome state? 4) How do miraciids detoxify the consumed Trichodesmium especially T. thiebautii ? Answering the above questions would shed much needed light on the true role of Trichodesmium Comprehensive studies shoul d be conducted in areas where Trichodesmium constitutes a significant fraction autotrophic production, especially during blooms. Possible aspects to investigate include analysis of stable isotopic ratios and long chain polyunsaturated essential fatty acids along with extensive laboratory experiments to conclusively establish feeding and reproductive habits of miraciid copepods and to unequivocally prove or disprove the link with Trichodesmium

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107 Figure 3 1 Integrated temperature (C) for various depth horizons at BATS (1995 1999) 16 18 20 22 24 26 28 30 11 Jan 16 Mar 26 Apr 12 Jun 18 Aug 10 Oct 15 Dec 14 Feb 15 Mar 9 Apr 7 May 8 Jul 2 Sep 5 Nov 13 Jan 6 Feb 4 Mar 8 Apr 11 Jun 11 Aug 6 Oct 9 Dec 11 Feb 9 Mar 7 Apr 2 Jun 10 Aug 22 Oct 7 Dec 27 Jan 23 Feb 7 Apr 1 Jun 3 Aug 11 Oct 8 Dec 1995 1996 1997 1998 1999 Temperature 0 20m integrated cruise Temp 0 50m integrated cruise Temp 0 100m integrated cruise Temp 0 200m integrated cruise Temp

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108 Chapter Four BATS 64 200 m Size Category Zooplankton Community Structure: Seasonal, Inter annual Patterns and Ecology, with Emphasis on Non Calanoid Copepods

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109 Introduction The classical food chain of diatoms to copepods to fish was the prevailing model of pelagic ecology for a good portion of the annals of biological oceanography. The realization that microbial auto and heterotrophs dominate production and metabolism in the open ocean occurred rather late in the history of ocean research when Pomeroy (1974) invoked a new paradigm the potential supremacy of microbial processes in the pelagic realm. The paradigm shift was a direct result of new methods for assessing bacterial populations, notably the introduction of epifluorescent techniques (Miller, 2004). A decade later 2 m) and free living heterotrophic bacteria feeding on DOM and are consumed by heterotrophic nanoflagellates (2 20 m) that are in turn fed upon by microflagellates, ciliates and micro metazoans in the size range of 20 200 m while DOM released from phytoplankton as exudates and from zooplankton through sloppy feeding and leaching from fecal pellets is consumed by bacteria and excreted N is utilized by the picoautotrophs in an efficient cyclical manner. The microbial loop is particularly important in oligotrophic o pen ocean systems such as BATS. Microzooplankton in the size range of 64 200 m (i.e. retained between 200 and 64 m screens) are dominated, in terms of biomass and abundance, by adults of small copepod species, and larval stages of both small and larger t axa (Deevey, 1971; Hopcroft, 1998; Paffenhfer and Mazzocchi, 2003; Turner, 2004). While the great majority of pico auto and heterotrophic biomass is consumed by nano heterotrophic flagellates (Paffenhfer, 1998; Landry and Calbet, 2004; Calbet and Land ry, 2004) micro metazoans are, nonetheless, vital intermediaries in terms of trophic transfer of carbon and recycling of nutrients in the photic zone. They are particularly important to the shunting of energy out of the microbial loop and into larger anima ls at higher trophic levels (Hopcroft and Roff, 1998a, 1998b; Hopcroft et al., 1998; Gallienne and Robins, 2001). This is particularly significant in oligotrophic oceans, such as the Sargasso Sea, where picoautotrophs dominate primary production and the mi crobial loop largely controls the fate of energy and elements in the euphotic zone. For example, Roff et al. (1995) have shown the ability of nauplii to ingest fluorescently labeled bacteria thus demonstrating their capacity to transfer energy from the mic robial loop to higher trophic levels, as nauplii are a main food source for many larger metazoans,

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110 particularly mesozooplankton. Coupled with their extremely high abundance and relatively high growth rates, nauplii may be an important and overlooked second ary producer in the open ocean (Hopcroft and Roff, 1998a). Unfortunately, in spite of their ecological importance, micro metazoans are severely understudied compared to larger zooplankton (e.g. meso and macro zooplankton), particularly with regard to rate measurements. This is due to the methods use d to sample the 64 200 and the > 200 m zooplankton. Traditionally, microzooplankton have been s ampled using water bottles and mesozooplankton by nets with mesh 200 m. The two methods largely neglect the metazoans in the size range of 100 800 m in linear dimension, as this size category is mostly extruded through the plankton nets used and severely under sampled by the 30 liter water bottles typically used to sample the microzooplankton (Hopcroft et al., 2001). More recent studies spanning nearly all oceans and latitudes have shown that micro metazoans dominate the larger mesozooplankton in terms of both abundance and ecological rate processes (Calbet et al., 2001; Satapoomin et al., 2004; Thor et al ., 2005; Zervoudaki et al., 2007; Jyothibabu et al., 2007). For example, the very small Microsetella norvegica has been found to be associated with aggregated organic material such as discarded larvacean houses in the ocean (Alldredge, 1972; Steinberg et al., 1997) and have been shown to feed on these aggregates (Uye and Onb 2002; Koski et al., 2005 and 2007; Maar et al., 2006). As a consequence, it is thought that Microsetella spp have an important role in the pelagic ecology where it is found (Uye and Onb, 2002; Koski et al., 2005) including the BATS site. Very few studies have been conducted on the 64 200 m metazoans in the BATS region. Bttger Schnack (1982) and Paffenhfer and Mazzocchi (2003) examined abundance while biomass estimates were made by Roman et al. (1993, 1995). The present study aims to investigate the importance of the micro metazoans mainly copepods and their larvae to the community structure in terms of abundance, biomass as well as species diversity and to the ecology in terms o f C and N dynamics at BATS.

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111 Materials and Methods Sample c ollection In addition to the day night 200 m mesh net samples collected during each BATS cruise, a single night tow (Taylor tow) was conducted using a 0.5 m diameter net with 20 m (1995 1996) and 35 m mesh for 1997. The net was towed to a depth of 150 m and was fitted with a flowmeter (General Oceanics) seawater solution alone while the other ha lf, in addition to buffered formalin seawater solution, had SrCl added to preserve Acantharia. A total of 36 tows were analyzed. Community structure analysis p rocessing Between 1/8 to 1/32 o f each Taylor tow was wet sieved through 3 me shes (200, 64 and 20 m) to produce 3 nominal size classes of >200 m, 64 200 m and 20 64 m. This approach was used to assess the differences between animals retained by a 200 m mesh and those that pass through, and to compare similar size fractions gat hered from the different meshes used to collect samples in 1995 1996 (20 m mesh net) relative to those gathered in 1997 (35 m net). The entire zooplankton community of the Taylor tows was enumerated. Each sample > 200 m and the 64 200 m fractions were analyzed. All abundance values are from the smaller size fraction of 64 200 m. The > 200m category was used to calculate net capture efficiencies of the different net systems used at BATS. The entire sieved sub sample was analyzed for the > 200 m fract ion while the 64 200 m fraction was further split into smaller sub samples. Generally, 1/16 to 1/256 of the entire tow was analyz ed for the 64 200 m size class with the aim of counting at least 100 individuals of the most common non calanoid genus. On av erage, 487 (258 to 1,2 01) non calanoids were enumerated while an average of 265 (71 to 784) calanoid copepods were counted and a mean of 1,407 (624 to 4238) copepod nauplii were enumerated from the 64 200 m size fraction.

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112 The zooplankton counted for the > 200 m fraction were processed in an identical fashion as the BATS samples (i.e. all non calanoid copepods and larvaceans) while all metazoans were enumerated for the 64 200 m size class. Estimates of biomass and carbon nitrogen cycling by microzoopla nkton To enable comparisons with studies conducted in the past on microzooplankton (i.e. 64 200 m size fraction) as well as to understand their role in C and N cycling, it was imperative to arrive at reasonable biomass estimates of the animals found in t hi s size category at BATS. B iomass was not measured directly in the present study. However, dry weight of all copepod species and stages (including nauplii) were estimated using results of several published studies. Each zooplankton category was assigned a biomass value depending on the average linear size of the a nimals compo sing it Between 100 and 20 animals were measured (nauplii n = 100 and most other groups 20 40 animals). The estimated biomasses per category (Table 22) were used along with ambient temperatures for the upper 150 m of the water column at the time of sample collection in order to calculate respiration and excretion using the equations of Ikeda. Table 22 Estimated biomass for the average constituent of each category and species of cope pod present in the 64 200 m size category at BATS A long with the average linear dimensions of animals within a particular group (total or prosome length in m), and the source of the estimate Group/species Biomass estimate (g dwt ind 1 ) Mean body length (m) standard deviation Reference Copepod nauplii 0.014 112 53 (*TL) Hopcroft et al. (1998) Calanoid copepodites 0.454 257 115 Webber and Roff (1995) Adult calanoid spp. 1.23 403 163 (PL) Microsetella rosea 2.5 715 210 (TL) Uye and Onb (2002) M. norvegica 1.0 445 64 (TL) Microsetella spp. copepodites 0.5 3 11 77 (TL) Oncaea scottodicarloi 1.39 Mean biomass for adults Bttger Schnack and Dietrich Schnack (2005) Oncaea spp males 1.39 Triconia minuta 1.78 T. dentipes 1.06 O. zernovi 0.405 Spinoncaea ivlevi 0.283 O. atlantica 0.153 O. vodjanitskii 0.153

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113 Table 22 (continued) Group/species Biomass estimate (g dwt ind 1 ) Mean body length (m) standard deviation Reference Large Oncaeid copepodites 0.151 202 33 (PL) Webber and Roff (1995) Small Oncaeid copepodites 0.647 113 24 (PL) Oithona spp. 0.206 197 38 (PL) ** Corycaeid copepodites 0.332 243 50 (PL) Webber and Roff (1995) Farrannula rostrata males 1.19 421 15 (PL) Webber and Roff (1995) *TL=Total Length ** Average of Chisholm and Roff (1990), Webber and Roff (1995), Hopcroft et al. (1998) and Satapoonin (1999) Estimation of Microsetella spp. carbon demand Microsetella spp. carbon demand (CD) was estimated using three independent methods. The first was by using the weight specific grazing rates calculated for M. norvegica in the study of Koski et al. (2007). Koski et al. found M. norvegica to ingest 16% of body carbon per da y feeding on discarded larvacean houses at 15C. The proceeding rates were adjusted to the mean temperature of the upper 150m at BATS using a Q 10 of 2. The other approach used to estimate carbon requirements of Microsetella spp. was by employing separate t emperature adjusted rates of production for M. norvegica adult females and copepodite stages calculated by Uye and Onb (2002). Microsetella spp. were not separated by sex in the present study but a ratio of 1:1 for females and males was assumed for the pu rposes of calculating production (most other harpacticoid species in the present study had sex ratios close to 1:1) The final technique employed to estimate total carbon demand was to calculate respiration rate and to assume that it made up 40% of total c arbon requirements (Roman et al., 2002). From the length weight regression of Uye and Onb (2002) an average individual carbon biomass of 1.0, 0.4 and 0.2 g was used for Microsetella rosea M. norvegica adults and copepodites, respectively. These were rea sonable approximations as they represented a total body length (excluding the very long caudal setae) M. rosea adults of just over 700m and M. norvegica adults and copepodites of approximately 450 and 300 m, respectively which fit what was observed during the plankton analysis.

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114 The next key piece of information needed in estimating the role of Microsetella spp. in aggregate consumption was to get an idea of marine snow production in the upper 150m at BATS L arvacean house production was used as a simple proxy for aggregate formation. Using the same methods employed in chapter 1 (i.e. rates of Sato et al., 2003) temperature specific house production rates larvaceans were utilized at BATS. Statistical m eth ods All annual and seasonal comparisons were performed using the non parametric Kruskal Wallis test of medians as well as post hoc multiple comparisons of ranks. This was due to the non normal distribution of much of the data and the small sample size of some of the comparisons (e.g. summers and falls only had 6 and 7 tows, respectively). Determination of relationships between zooplankton abundance and other biological parameters at BATS was by wa y of Spearman Rank correlation analysis (non parametric analog of Pearson product moment correlation coefficient). Results Tow statistics Overall, 36 net tows using very fine mesh sizes (20 35 m), representing 36 BATS cruises (1995 1997), were analyzed in the present study. In th is section of the paper all 200 m net tows will be termed as follows: 10 in 1995, 12 in 1996 and 14 in 1997. Seasonally, there were 13 winter, 10 spring, 6 summer and 7 fall tows taken during the 3 year study period. Volumes filtered are detailed in Appendix 5. The maximum depth of nearly all tows was 150 m with only 2 tows deviating from this number. However, the volume of seawater filtered varied conside rably averaging 27 m 3 with a standard deviation (s.d.) of 16. From annual averages it appeared that 1997 had a higher mean volume filtered with 32 m 3 (16) versus 27

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115 (20) and 21 m 3 (9) for 1995 and 1996, respectively. Pooled seasonal values showed winter a nd fall with highest volumes filtered, on average, corresponding to 33 (18) and 32 m 3 (17) and lowest volumes of 22 (13) and 18 (7) in spring and summer, respectively. However, upon analysis (Kruskal Wallis test), no significant differences were detected a mong years or seasons in terms of volumes filtered. This was the case in spite of the fact that 1997 tows were conducted using a net with larger mesh size (35 vs. 20 m). In addition, Appendix 5 lists the average portion of each of the 2 size fractions (> 200 and 64 200 m) counted for each year as well as season (pooled). Overall, between 1/32 and 1/8 of the entire tow were analyzed for the larger fraction and 1/256 to 1/16 for the smaller size class. General community s tructure In addition to the comm unity found in the BATS 200 m zooplankton tows, the fine mesh nets used in gathering the Taylor tows were expected to capture mostly copepod larvae (nauplii and copepodites) and other zooplankton developmental stages. Also, it was anticipated that some of the smaller adult copepods would be sampled in greater numbers due to presumed escapement of the smaller species through the larger pore sizes of the 200 m mesh net. However, an astonishing array of adult microcopepods was found in the 64 200 m fraction of the Taylor samples analyze d. Table 23 lists the major groups and species found along with overall average, range and seasons of maximum abundance at BATS. The most numerous group, by far, were copepod nauplii (Figure 31). They had an overall average abundance of nearly 7.5 x 10 5 individuals per m 2 that represented 60% of all zooplankton numbers over the entire study period (1995 1997). Nauplii were followed, in terms of overall abundance, by Oncaeidae adults and copepodites averaging 1 53 x 10 5 individuals per m 2 making up just over 12.5% of zooplankton contained in the 64 200 m size category. Next, in terms of numerical dominance were copepodites of calanoi d copepods (Figure 32) with 1 21 x 10 5 copepods m 2 that represented nearly 10% of total zooplankton numbers. Adult calanoid copepods (mostly Paracalanidae and Calocalanidae spp.) as well as Oithona spp. (Figure 33), Microsetella spp. and Corycaeid adults and copepodites (Figure 34) rounded out the copepods in terms of population numbers and they composed an overall of 1.25, 6.20, 1.94 and 0.42%,

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116 respectively, of total zooplankton abundance at BATS from 1995 to 1997. Other non copepod zooplankton found in t he 64 200 m fraction included, in order of abundance and consisting of at least 0.1% of total zooplankton, were larvaceans (Figure 35), radiolaria, tintinids, gastropod larvae, foraminifera, ostracod larvae and polychaete larvae making up 3.8, 0.97, 0.86, 0.59, 0.34, 0.22 and 0.11% of all zooplankton enumerated (Table 23 ). The non calanoid copepods found in the 64 200 m size category included many adult species found either entirely or overwhelmingly in this fraction. The most important were members of th e genera Microsetella and Oncaeidae (including Oncaea Triconia and Spinoncaea ). Microsetella consisted of two species, M. rosea and M. norvegica (Figure 36). Adults of these species were present in some BATS samples but in much lower ov erall numbers (819 vs. 5 and 1.4 5 x 10 4 vs. 2 copepods m 2 for M. rosea and M. norvegica respectively). The Family Oncaeidae within the 64 200m fraction contained seven id entified and one unidentified species These were, in order of overall abundance (individuals m 2 ) O. zernovi (3 3 x 10 4 Figure 37), Spinoncaea ivlevi (2 2 x 10 4 Figure 37), Triconia dentipes (6 x 10 3 Figure 38), O. atlantica (5 x 10 3 Figure 39), Oncaea spp males (5.2 x 10 3 Figure 40), O. vodjanitskii (1.1 x 10 3 Figure 39), O. scottodicarloi fema les (941, Figure 40), Triconia minuta females (926, Figure 38) and Oncaea sp 1 (326 copepods m 2 ). Ta ble 23 Taylor net zooplankton (64 200 m) taxa enumerated with overall mean individual abundance m 2 (0 150 m) and seasons of maximum numbers Group Species Overall abundance Average Range Season(s) of maximum numbers Copepod nauplii 740 x 10 3 103 1391 x 10 3 Spring Calanoid copepodites 121 x 10 3 34 289 x 10 3 Winter Calanoid copepods Clausocalanus spp. 30 0 745 Winter and Fall Paracalanus spp. 4 x 10 3 0 26 x 10 3 Fall Calocalanus spp. 3.3 x 10 3 0 25 x 10 3 Winter and Spring Ectinosomatidae Microsetella rosea 819 0 3865 Summer and Fall Microsetella norvegica 14.5 x 10 3 0 51 x 10 3 Summer Oncaeidae 941 0 3653 Spring and Summer Mixed Oncaea 5.2 x 10 3 0 37 x 10 3 Spring 926 0 3 x 10 3 Summer and Fall T. dentipes 6 x 10 3 0 30 x 10 3 Fall Spinoncaea ivlevi 22 x 10 3 0.75 80 x 10 3 Fall Oncaea atlantica 5 x 10 3 0 33 x 10 3 Fall O. zernovi 33 x 10 3 4.5 82 x 10 3 Winter and Spring O. vodjanitskii 1.1 x 10 3 0 5.8 x 10 3 Spring, Summer and Fall Oncaea sp1 326 0 2.2 x 10 3 Fall

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117 Table 23 (continued) Group Species Overall abundance Average Range Season(s) of maximum numbers Corycaeidae 147 0 1.3 x 10 3 Spring Pontoeciellidae 69 0 1.3 x 10 3 Spring 245 0 2.4 x 10 3 Summer Mormonillidae Sapphirinidae 58 0 891 Spring, Summer and Fall Oithonidae Oithona spp.* 78 x 10 3 18 163 x 10 3 Winter and Spring Non copepod zooplankton Larvaceans 46 x 10 3 2 197 x 10 3 Year round Radiolaria 12 x 10 3 1.7 29 x 10 3 Year round Foraminifera 4.1 x 10 3 0 26 x 10 3 Fall and Winter Tintinids 10.6 x 10 3 0 55 x 10 3 Spring Gastropod larvae 7.2 x 10 3 0 23 x 10 3 Spring and Summer Pelycepod larvae 45 0 670 Summer Chaetognath larvae 644 0 3.6 x 10 3 Spring Mesusa larvae 837 0 7.6 x 10 3 Spring Echinoderm larvae 408 0 3.4 x 10 3 Fall and Winter Polychate larvae 1.4 x 10 3 0 9.2 x 10 3 Fall Doliolid larvae 135 0 1.3 x 10 3 Summer Ostracod 2.8 x 10 3 0 8.1 x 10 3 Fall Creisis 422 0 13 x 10 3 Spring Salp larvae 99 0 1.2 x 10 3 Spring Siphonophore 39 0752 x 10 3 Fall and Winter Barnacle nauplii 34 0 1.2 x 10 3 Fall Amphipod larvae 11 0 390 Spring Includes copepodites Of these only Oncaea spp males, O. scottodicarloi Triconia minuta and T. dentipes were ever found in BATS 200 m mesh nets. Not one individual from the other species listed above was ever found in any of the 131 BATS 200 m samples. This was no doubt due to the very small size of these adult m in total length and some species were barely 200 m in body length. In addition to adults, Oncaeidae copepodites (Figure 41) were found in very large numbers These copepodites were separated into 2 size categories: large (>300 m) and small (< 300 m). Overall abundance of large oncaeid copepodites averaged 7.9 x 10 3 individuals m 2 while the small category had a grand mean of 7 .1 x 10 4 copepods m 2 Other species of non calanoid copepods included Mormonilla minor Farranula rostrata males, Pontoecielia abyssicola copepodites and Corissa parva copepodites with overall mean abundances of 245, 147, 69, and 58 individuals m 2

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118 Figure 32 Copepod naupl ii abundance individuals m 2 (0 150 m) from 64 200 m size fractions at BATS ( 1995 1997 ) 0 200,000 400,000 600,000 800,000 1,000,000 1,200,000 1,400,000 1,600,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Copepod nauplii

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119 Figure 33 Calanoid copepod abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 50,000 100,000 150,000 200,000 250,000 300,000 350,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Calanoid copepodites Calanoid adults

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120 Figure 34 Oithona spp. abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 20,000 40,000 60,000 80,000 100,000 120,000 140,000 160,000 180,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Oithona spp. Oithona spp.

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121 Figure 35 Corycaeid copepodite abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 2,000 4,000 6,000 8,000 10,000 12,000 14,000 16,000 18,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Corycaeid copepodites

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122 Figure 36 Larvacean abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 50,000 100,000 150,000 200,000 250,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Larvaceans

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123 Figure 37 Microsetella spp. abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 10,000 20,000 30,000 40,000 50,000 60,000 70,000 80,000 90,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Microsetella rosea Microsetella norvegica Microsetella spp. copepodites

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124 Figure 38 Oncaea zernovi and Spinoncaea ivlevi abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 10,000 20,000 30,000 40,000 50,000 60,000 70,000 80,000 90,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Oncaea zernovi Spinoncaea ivlevi

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125 Figure 39 Triconia minuta and T. dentipes abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 5,000 10,000 15,000 20,000 25,000 30,000 35,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Triconia minuta T. dentipes

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126 Figure 40 Oncaea atlantica and O. vodjanitskii abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 5,000 10,000 15,000 20,000 25,000 30,000 35,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Oncaea atlantica O. vodjanitskii

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127 Figure 41 Oncaea scottodicarloi and Oncaea spp. (male) abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 5,000 10,000 15,000 20,000 25,000 30,000 35,000 40,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Oncaea scottodicarloi Oncaea spp.

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128 Figure 42 Oncaeidae copepodite abundance, individuals m 2 (0 150 m) from 64 200 m size fractions at BATS (1995 1997). 0 20,000 40,000 60,000 80,000 100,000 120,000 140,000 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Copepods per square meter (0 150 m) Small (<300 microns) Large (>300 microns)

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129 Annual t rends The overall annual trend was for higher zooplankton abundance in 1995 vs. 1996 and 1997, similar to results of 200 m net samples. Appendix 6 and 7 lists annual abundance statistics for major constituents of all zooplankton in the 64 200 m size fractions Most copepod groups and species had highest abundance in 1995, with some notable exceptions. Copepod nauplii, the most numerous component, had relatively stable numbers among the years analyzed as did Microsetella spp ., both as a genus as well as separat ed into its two constituent species. Other zooplankton components had different years of peak abundance. For example, Mormonilla minor and Farranula rostrata males were found in greater numbers in 1996 than either 1995 or 1997, although the numbers found were quite low. Adult calanoid copepods, on the other hand, had significantly higher abundance in 1997 compared to either 1995 or 1996 (Table 24 ) The year 1997 was also the time of highest numbers of echinoderm larvae, while 1996 was the year of peak abun dance for gastropod, chaetognath and polychaete larvae. The most marked annual differences among the Oncaea species and copepodites were found in oncaeid copepodites (< 300 m), Oncaea zernovi Oncaea spp males and Triconia minuta All of those groups and species had significantly higher abundance in 1995 (Table 24 ) In general, the previous results agree with those found for the BATS 200 m mesh net samples non calanoid groups. Table 24 Statistically significant differences between years for 64 200 m size fraction zooplankton (1995 1997) Family Species Annual difference Multiple comparisons p values Kruskal Wallis p value Calanoid copepods 1997 > 1996 0.037 0.044 Oncaeidae Mixed Oncaea 1995 > 1996 and 1997 0.028 and 0.021 0.011 1995 > 1996 0.050 0.050 O. zernovi 1995 > 1997 0.016 0.020 Oncaeid copepodites (<300m length) 1995 > 1996 0.029 0.029

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130 Seasonal p atterns Non calanoid copepods in the 64 200 m size fractions were generally least abundant in winter with the exception of Spinoncaea ivlevi Oncaea zernovi and Oithona spp which all had their abundance ebb in summer. Appendix 8 and 9 summarizes all seasonal abundance data for major constituents of the 64 200 m zooplankton of all Taylor tows Species of Oncaeidae the most numerous copepod family in the 64 200 m size fraction, exhibited varied seasonal abundance patterns. The dominan t species O. zernovi showed the most pronounced seasonal variability among members of Oncaeidae in the size fraction with highest numbers during winter and spring and lower abundance in summer and fall (3.9 and 4.1 vs. 2.0 and 2 3 x 10 4 m 2 respectively ) with statistically significant differences be tween spring and summer (Tale 25 ) The next most numerous species, Spinoncaea ivlevi had a different seasonal pattern than O. zernovi with a relatively stable population from wint er through summer (range = 1.8 to 2.2 x 10 4 m 2 ), that peaked in fall (3 0 x 10 4 m 2 ). Triconia dentipes the third most important oncaeid species in terms of abundance, had a gradual buildup in population from the low in winter to the maximum in fall (4.7 vs. 8.6 x 10 3 m 2 ). Following T. dentipes were Oncaea spp males (most likely those of O. media and / or O. scottodicarloi ). They had a pattern of peak abundance in springtime (8.8 x 10 3 m 2 ) about twice the numbers of any other season. Oncaea atlantica was most numerous during summer and fall and least in winter and spring (5.8 and 10 vs. 2.9 and 3.7 x 10 3 m 2 ). Rounding out the species of Oncaeidae identified in the 64 200 m fraction were O. vodjanitskii O. scottodicarloi (females) and Triconia minuta All of the previous species had lowest abundance during winter but varied in the season of highest abundance. O. scottodicarloi females were most abundant during spring and summer whereas both Triconia minuta and Oncaea vodjanitskii were relati vely stabl e from spring to fall. The last group of the family Oncaeidae analyzed was the copepodite stage. This stage was split into 2 categories based on size (small < 300 and large > 300 m body length) The large category was far less abundant in summer with 5.4 x 10 3 m 2 (about 60% less than all other seasons) while the other seasons had very similar abundances (within 5%). The pattern for the small size category was slightly different with a springtime peak abundance of 8 .6 x 10 4 m 2 and a summer minimum of 5.4 x 10 4 m 2

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131 In the case of the second most numerous non calanoid taxa Oithona spp. the seasonal trend for was for high numbers in winter and spring and lower abundance in summer and fall (8 .0 and 9.2 vs. 5.7 and 6 .4 x 10 4 m 2 ) Combined abundances of adults and copepodites of the genus Microsetella the third most numerous non calanoid copepod in the 64 200 m size fraction, showed the strongest seasonal differences among all non calanoid genera examined, with significantly highe r (Table 25) abundance in spring, summer and fall compared to winter (4.0 3.0, and 2.7 vs. 1.1 x 10 4 m 2 respe ctively ). H owever, when the adults of the two constituent species of the genus were analyzed separately it was noted that, while both had high summer densities they differed in onset and decline of their peak population with Microsetella norvegica peaking earlier and M. rosea maintaining its high abundance through fall (figure 36). Other groups and species of non calanoid copepods present in suf ficient numbers to justify analysis were Corycaeid copepods and Mormonilla minor Corycaeid copepods, represented almost exclusively by copepodites, were about 3 times less abundant in winter (2.3 x 10 3 m 2 ) than all other seasons and were present in similar numbers in spring through fall. This result was in line for that found for Corycaidae in the BATS 200 m net samples. The last species to be mentioned, Mormonilla minor had peak numbers in summer and lowest abundance in winter (400 vs. 100 copepod s m 2 ). Seasonal patterns of other zooplankton were also analyzed. The most numerous group, copepod nauplii, had higher abundance in spring and fall and lower numbers in winter and summer (8 .9 and 8 .1 vs. 6 .5 and 6.1 x 10 5 m 2 ). Calanoid copepodites, on th e other hand, had their highest densities in winter (1 .5 x 10 5 m 2 ) and lowest in spring and summer (1 .1 and 9 4 x 10 4 m 2 respectively). Total adult species of calanoid copepods were relatively uniform in their population numbers, varying less than 20% a mong seasons. The only non copepod crustacean category analyzed, ostracods, were found in highest numbers in spring and fall and lowest in winter. Seasonal trends of the most important non crustacean groups in the 64 200 m fraction were variable. Larvace ans had highest nu mbers in winter and summer (5.1 and 5.4 x 10 4 m 2 ) and lowest in spring (3.7 x 10 4 m 2 ). Radiolaria were relatively uniform in abundance from spring through fall varying by approximately 10% but were much lower in winter (> 40%) than any other season. Foraminifera, on the other hand, had a quite different pattern of seasonal abundance distribution with maximum populations in fall and winter and lowest in summer (~factor of 5 difference) and intermediate numbers in spring.

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132 Tintinnids and ga stropod larvae had the most pronounced seasonal differences with significantly higher abundance in spring and summer compared to winter (factor of 2 and 3 difference for tintinnids and gastropods, respectively). Table 25 0.05 level) differences between pooled seasons for 64 200 m size fraction zooplankton (1995 1997) Family Species Seasonal difference Multiple comparison p value Kruskal Wallis p value Ectinosomatidae Microsetella spp. (all) Spring > Winter Summer > Winter 0.027 0.008 0.003 Microsetella rosea Summer >Winter Fall > Winter 0.168 0.191 0.036 Microsetella norvegica Spring > Winter Summer > Winter 0.033 0.018 0.007 Microsetella copepodites Winter < Spring, Summer and Fall 0.036, 0.001 and 0.101 0.001 Oncaeidae O. zernovi Spring > Summer n.s 0.049 Corycaeidae Corycaeidae (all) Winter < Spring, Summer and Fall 0.019 and 0.113 0.009 Corycaeidae copepodites Winter < Spring and Summer 0.016 and 0.114 0.008 Tintinids Spring > Winter 0.024 0.030 Gastropod larvae Spring > Winter 0.027 0.024 n.s: not significant Relationship between zooplankton abundance and environmental f actors In an attempt to correlate environmental factors to zooplankton abundance in the small fraction (64 200 m) various biological parameters (e.g. primary production and plant pigments) integrated to 150m were analyzed. Results of Spearman Rank analysis between zooplankton in the 64 200 m size fraction of Taylor tows are shown in Table 26 Ve ry few parameters showed any significant correlations with any zooplankton taxa analyzed. Primary production sediment trap POC flux at 150 m, and suspended POC was not significantly correlated with any of the eleven zooplankton taxa analyzed. However, all three of the phytoplankton pigments analyzed showed a few cases were the correlation was significant. Chlorophyll a had significant correlations with foraminifera and Microsetella spp Although, the

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133 relationships differed in sign, with foraminifera having a positive relation and Microsetella spp. a negative relationship with Chlorophyll a (Table 26 ). Furthermore Microsetella spp also had a significant positive correlation with the accessory pigment p eridinin (indicative of dinoflagellates) along with gastropod larvae. Finally, the accessory pigment fucoxanthin (representing diatoms) was significantly corr elated with tinitinds. Table 26 Significant (p < 0.05) results of Spearman Rank correlation analy sis between selected zooplankton taxa from the n Taylor (64 200 m) size fraction abundance m 2 (0 150 m) and various biological parameters measured during the same cruise integrated to 150 m depth at BATS (1995 1997) Environmental parameter Zooplankton taxa R value P value Primary production (mg C m 2 d 1 ) No significant results 0.34 n.s Sediment trap POC 150 m (mg C m 2 d 1 ) No significant results n.s Suspended POC (mg C m 2 ) No significant results n.s Chlorophyll a (mg m 2 ) Microsetella spp 0.34 0.043 Foraminifera 0.43 0.008 Fucoxanthin (g m 2 ) Tintinids 0.36 0.033 Peridinin (g m 2 ) Microsetella spp 0.38 0.021 Gastropod larvae 0.34 0.045 Copepod b iomass in the 64 200 m size fractions Overall biomass for the Taylor copepod fraction (64 200 m ) amounted to 177 mg dwt m 2 while the average for the BATS samples taken on the same cruises was 400 mg dwt m 2 Therefore, the 200 m net missed close to 50% of the metazoan biomass at BATS in the upper 150 m. Comparisons revealed a consistent pattern of biomass among seasons for the 64 200 m with averages of 169, 189, 159 and 178 mg dwt m 2 for winter, spring, summer and fall. However, there were greater annual differences in dry weight estimates with 215, 148 and 174 mg dwt m 2 for 1995, 1996 and 1997, respectively. The situation was

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134 reversed in the case of the > 200 m zooplankton samples with more pronounced seasonal than annual differences in biomass, the highest found in spring (514 mg dwt m 2 ) and lowest in winter (292 mg dwt m 2 ). Figure 42 shows the annual and seasonal pattern of biomass as distributed among the various size classes. Figure 43 Biomass (dry weight) distributions amon g all 5 BATS size fractions (0 15 0 m) and estimates for (0 150 m) 64 200 m Taylor fraction (1995 1997) The dominant contributors to biomass in the 64 200 m were calanoid copepods composed mainly (73%) of copepodite stages and to a lesser extent adults of small species (mostly paracalanids and calocalanids). Figure 43 illustrates the percentage contribution of the main groups of copepods to the biomass of the 64 200 m size fraction of BATS zooplankton. Calanoids contributed an overall of 42% of the biomass in t he 64 200 m category. This proportion remained fairly constant among years with a slightly higher proportion in 1997 mostly as an increase in small adult calanoid species. However, a notable 0 200 400 600 800 1,000 1,200 11 Jan 14 Feb 16 Mar 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 mg dry weight per square meter 64 200 m 200 500 m 500 1000 m 1000 2000 m 2000 5000 m >5000 m

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135 seasonal pattern emerged with calanoids making up half of the ca sharply in spring to 34% before rebounding slightly to 38 and 40% in summer and fall, respectively. The winter spike in calanoid biomass was mainly due to increas es in copepodite stages. Micro o ncaeid species (< 500 m in length including Triconia minuta T. dentipes Oncaea zernovi Spinoncaea ivlevi O. atlantica and O. vodjanitskii ) were second in importance to calanoids in terms of biomass, making up an overall 16% of the total. However, the largest differences in bot h absolute and relative biomass for the micro oncaeids were the result of annual change. The year1995 had nearly double the biomass of the other 2 years examined (44vs. 23 and 22 mg dwt m 2 ) composing a respective 20, 16 and 13% of 1995, 1996 and 1997 tota l biomass while the numbers were relatively consistent between seasons with a slight decrease in summer (23 vs. 28, 31 and 31 mg dwt m 2 ) making up 14, 16, 17, and 17% for summer, winter, spring and fall, respectively. Other components of the family Oncaei dae present in the microzooplankton fraction termed medium oncaeids (> 0.5mm) composed of Oncaea scottodicarloi and unidentified adult male species made up an average of 5% (8.6 mg dwt m 2 ) of total copepod biomass in the size fraction. The annual pattern was the same as that found for the micro oncaeids (1995 highest absolute and relative biomass), however, the seasonal difference was largely due to a nearly a doubling of biomass in spring compared to the rest of the seasons (13.7 vs. 6.1, 6.3 and 7.6 mg dwt m 2 representing 7.2, 3.5, 3.9 and 4.3% for spring winter, summer and fall, r espectively). Rounding out the o ncaeid group were the copepodite stages. They represented the 4 th most impor tant group relative to copepod biomass in the microzooplankton at BATS for all samples analyzed (9%). Oncaeid c opepodites as a group were very consistent in the relative contribution they made to copepod biomass in the 64 200 m fraction among the years an d seasons examined, with only a slight increase in spring and a small decrease in summer noted. It is i nteresting to note that if all o ncaeid adult and copepodite species were grouped together they would contribute a total of 30% of total copepod biomass i n the 64 200 m size fraction. Thus, in the < 200 m category, oncaeid copepods dominate the non calanoid copepods in terms of biomass contributing more than half of the biomass (57%) of this group. Microsetella spp were another important component of c opepod dry weight in the microzooplankton fraction and were the 3 rd after micro oncaeids in terms of their total contribution to biomass in the < 200 m size fraction, making up an average of 12% for all samples examined. Annual

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136 differences were slight, ho wever, seasonal distinctions were noted with winter containing the lowest absolute and relative quantities of biomass in the microzooplankton at BATS (9.7 mg dwt m 2 and 6%) and the highest in spring (34 mg dwt m 2 and 21%). Figure 44 Percent contribu tion of main species and groups to overall copepod biomass (64 200 m size fraction integrated to 150 m) at BATS for all Taylor tows ( 1995 1997 ). Following Microsetella spp in importance to biomass were Oithona spp They were largely made up of copepodite stages with some small adult species that together made up an overall of 9% of the total dry weight of copepods i n the microzooplankton fraction Seasonally, Oithona spp had its lowest contribution to biomass in s ummer (11.7 mg dwt m 2 vs. 18.4 mg dwt m 2 for spring). Finally, Corycaeid copepodites made up 1% or less of overall annual or seasonal biomass, while all other adults and larval stages together contributed to ~ 1% or less of total dry weight of the entire size category of 64 200 m. 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1995 1997 Others Corycaeid copepodites Oithona Oncaeid copepodites Micro oncaeids medium oncaeids Microsetella spp. Calanoids Calanoid copepodites Copepod nauplii

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137 Microzooplankton C and N dynamics at BATS One main reason for estimating individual copepod biomass was the fact that they composed the vast majority of the abundance and biomass in the microzooplankton sized 64 200 m, even more than in the mesozooplankton size category (Deevey 1971). In addition using the parameters already at hand (i.e. abundance and ambient water temperature) an estimation of the role of micro copepods in C and N cycling at BATS was possible. Comparing overall results (1995 1997) of the C demand (CD) of total copepods, includi ng copepodites and nauplii, in t he 64 200 m size fractions to > 200 m net bulk zooplankton already presented in chapter1 revealed the former to average 64.0 and the latter 47.9 mg C m 2 d 1 for the upper 150 m of the water column at BATS. Together these two values represented approximately 22% (25.2% if mesozooplankton was integrated to 200m) of average primary production measured at the same time as the zooplankton. Hence, although the microzooplankton biomass estimate is less than half (~ 45%) of that measured for the >200 m net samples for the same cruises they have nearly twice the C demand of recycling. They composed an average of 4.41 compared to 2. 94 (3.92 integrated to 200 m) mg N m 2 d 1 respectively, for the micro and mesozooplankton categories in the upper 150m (1995 1997). This amounted to 5.7 and 3.8% (5.1% integrated to 200 m) of the N demand of concomitantly measured primary production (PP) for micro and mesozooplankton, respectively. This is another illustration of the high weight specific rate processes of the 64 200 compared to the > 200 m categories of zooplankton. Microzooplankton made up a much larger quantity of C and N cycling duri ng 1995 than in either 1996 or 1997 (Figures 44 a b ) mainly due, as previously mentioned, to the higher biomass fou nd in the microzooplankton size range along with fewer mesozooplankton in 1995 The annual pattern observed in C D was also exhibited in N exc retion. Therefore, the metazoans in the 64 200 m are not only on par with rate processes of the > 200 m zooplankton but can even surpass them at times. Finally, in terms of seasons the microzooplankton were more important than mesozooplankton in C and N dynamics in winter and slightly less during spring and summer and nearly equal in fall (see F igures 42 a b ).

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138 Figure 45 (a and b) Percentage of primary production potentially consumed to satisfy the C demand (a) as well as that supported by recycled N (b) from copepods in the 64 200 m and mesozooplankton > 200 m (1995 1997). Overall, annual, and seasonal estimates of respiratory C calculated for all the main categories of 64 200 m copepods are listed in Appendix 10 while Appendix 11 presents the same information on N excretion. Annual and seasonal patterns for both C and N dynamics of the 64 200 m copepod fractions 0% 3% 5% 8% 10% 13% 15% 18% 20% 23% Percentage of primary production supported by excreted N Mesozooplankton > 200 m N excretion Microzooplankton (64 200 m) N excretion 0% 5% 10% 15% 20% 25% 30% 35% 40% 45% 50% 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1995 1997 Meso and microzooplankton C demand as a proportion of primary production Mesozooplankton > 200 m C demand Microzooplankton (64 200 m) C demand

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139 were basically the same as those discussed above in detail for biomass. Figure 45 illustrates the percent contribution of the main components of the 64 200 m copepods to C and N cycling at BATS. The main difference between the biomass configuration among years and seasons and that of elemental dynamics of the microzooplankton at BATS was the greater contribution of the ve ry small but numerically dominant nauplii. Their contribution to biomass was between 4.8 and 6.7% of the total for all copepods among annual and seasonal averages, however, they composed a much higher proportion mainly at the expense of the contribution by the larger sized calanoid copepods of C and N cycling ranging between 10 and 14% of total elemental cycling of all copepod categories in the 64 200 m size fraction. Figure 4 6 Percent contribution of main species and groups to overall copepod C and N metabolism (64 200 m size fraction integrated to 150 m) at BATS for all Taylor tows ( 1995 1997 ) It should be pointed out that C D as a percentage of PP is only an upper bound. It is likely that the majority of mesozooplankton and even many of the large r species of metazoans in the 64 200 m size category are primarily consumers of heterotrophs one to several steps away from the picoplankton (< 2 m) sized autotrophs which dominate in oligotrophic ocean systems such as the Sargasso Sea. 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100% 11 Jan 14 Feb 1 Mar 16 Mar 10 Apr 11 May 13 Jun 13 Sep 10 Oct 15 Dec 30 Jan 27 Feb 15 Mar 28 Mar 23 Apr 6 May 11 Jun 9 Jul 6 Aug 9 Oct 5 Nov 11 Dec 14 Jan 27 Jan 7 Feb 20 Feb 4 Mar 18 Mar 9 Apr 5 May 10 Jun 16 Jul 12 Aug 11 Sep 8 Oct 9 Dec 1995 1996 1997 Others copepod taxa Oithona spp. Corycaeid copepodites Oncaeid copepodites Micro Oncaeids Medium Oncaeids Microsetella spp. Adult calanoids Calanoid copepodites Copepod nauplii

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140 Aggregate C graze d by Microsetella spp. at BATS Overall Microsetella spp. was found to consume 4% of discarded house carbon produced by larvaceans at BATS on a daily basis in the upper 150 m of the water column. The percentage varied annually but mainly due to differences in larvacean abundance 1995 had nearly twice the larvacean abundance of 1997and close to 40% more than 1996. This trend was also observed in the BATS 200 m ne t samples di scussed in chapter 2 Microsetella spp. abundance on the other hand was relatively stable among the three years analyzed. However, there were pronounced seasonal differences with both larvacean and Microsetella spp. population densities. Winter had the highest larvacean abundance while spring had the lowest. Summer and fall had intermediate values. The two species of Microsetella had slightly shifted peak abundances with M. norvegica exhibiting maximum numbers in sum mer and starting its decline in the fall while M. rosea started its abundance increase in summer and continued to maintain that level in fall Microsetella i n summer with only a quarter of those numbers found in winter. The combination of Microsetella and larvacean abundances and differing temperature s led to the proportions of discarded house carbon consumed by the small harpacticoid copepods that ranged from 3.1 to 5.6% on an annual basis and 1.5 to 6.7% seasonally (Table 27 ) Table 27 L arvacean house production (mg C m 2 d 1 ) and Microsetella spp. carbon demand (mg C m 2 d 1 ) for 64 200 m size fractions integrated to 150 m ( 1995 1997 ) Overall 1995 1996 1997 Winter Spring Summer Fall House production 73 98 76 54 86 50 78 79 Microsetella spp. C demand Production 1.18 1.20 1.13 1.20 0.45 1.21 2.17 1.63 Grazing 1.92 1.96 1.82 1.98 0.83 2.19 3.30 2.37 ** Respiration 5.76 5.89 5.46 5.93 2.49 6.68 9.86 7.01 Average of all methods 2.95 3.02 2.80 3.04 1.26 3.36 5.11 3.67 % of house production 4.0% 3.1% 3.7% 5.6% 1.5% 6.7% 6.5% 4.7% *Sato et al (2003) Uye and Onb (2002) Koski et al (2007) **Ikeda (1985)

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141 Net Capture Efficiencies of the two Net Types Employed at BATS In order to calculate possible underestimation of the smaller non calanoid copepods sampled by the 200 m net at BATS, a c omparison was made between the two size fractions of all Taylor tows (20 35 m 200 and 64 m screen to obtain two size classes (i.e. > 200 and 64 200 m). The > 200 m (large) size fraction was assumed to represent the zooplankton captured by a 200 m mesh net and the 64 200 m (small) category as the quantity that was missed by the same net. This was a reasonable assumption sinc e a cursory scan of the plankton that passed through the 64 m screen revealed them to contain mostly phytoplankton in addition to some small tintinids and cope pod nauplii and the occasional o ncaeid copepodite; all in much lower numbers than found in the 6 4 200 m size fractions. Attention was focused on those groups and species present to a lesser or greater degree in both size classes. Abundance calculated in each category was expressed as a percentage of the sum total of both size fractions for each non calanoid group and species. A total of 16 different species and groups of non calanoid copepods as well as a category for larvaceans were analyzed and represented specie s and groups found in both the > 200 and 64 200 m size fractions, and were subject to a possible underestimation by the BATS 200 m net system Overall, the total non calanoid abundance in the large fraction composed only 9.4% of the total found in both size categories (Table 28 ) This meant that, on average, the small mesh nets (20 and 35 m) captured nearly 10 times more non calanoid copepods (range = 4.7 to 18.3) than the 200m mesh net at BATS. However, it must be noted that this is only in terms of abundance and not biomass, as the smaller non calanoids, in most cases, contained muc h less biomass than the larger ones in the > 200 m size fraction. Annually, the fraction of non calanoid abundance passing through the 200 m mesh was remarkably consistent (91.3 vs. 89.9 and 90.8%, for 1995, 1996 and 1997, respectively). However, differe nces were found seasonal ly with winter and spring as having slightly fewer non calanoid copepods in the larger fraction than either summer or fall (8.9 and 7.6% vs. 10.6 and 11.7%, respectively) with the difference between spring and both summer and fall b eing statistically significant (K W, p = 0.015, M.C, p < 0.05).

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142 Species of the family Oncaeidae had varying percentages of adult populations captured by the 200 m screen (a proxy for the BATS 200 m mesh net). Three species were analyzed; namely Oncaea s cottodicarloi females, Triconia minuta and T. dentipes (males and females examined separately), in addition to mixed males (composed of O. scottodicarloi and O. media ) and copepodites. Overall, approximately 70% of Oncaea scottodicarloi females were retain ed by the 200 m mesh whereas just under half (48%) of Triconia minuta females were captured by the 200 m mesh net. The percentage dropped precipitously in the case of T. dentipes with fewer than 5% of adult females and just 0.04% of adult males held by t he 200 m screen. Slightly less than (23%) of the overall Oncaea spp. mixed male category were retained by the 200 m mesh screen. Finally, nearly 99% of all Oncaea spp copepodites passed through the 200 m screen (Table 28 ) While it was anticipated that a large percentage of Oncaea spp copepodites would be missed by the 200 m mesh net, this was nevertheless a surprising result. When the proportions of Oncaea spp copepods retained by the 200 m screen were grouped by yea rs, none exhibited statistically significant differences (K overall pattern was for a greater proportion of copepods to pass through the 200 m screen during spring than any other season with the exception Oncaea scottodicarloi females which had a higher percentage of the population in the 64 200m size fraction in summer. Triconia dentipes had a significantly greater proportion of adults in the small fraction in spring than other seasons (K W, p = 0.03). It shou ld be noted that the above comparison of oncaeid numbers, retained by the 200 m screen after wet sieving, did not include adult Spinoncaea ivlevi Oncaea zernovi O. atlantica or O. vodjanitskii None of those species were ever captured by the 200 m scre en. Thus, it would seem that the BATS 200 m mesh net not only under samples a high proportion of many of the smaller oncaeid species but misses many entirely. As a whole, for all samples analyzed (1995 1997), fewer than 15% of all Oithona spp. (includ ing copepodites) remained on the 200 m screen. This included less than of adult males and an unknown but presumably (males are smaller than females) higher percentage of adult females. A slightly greater percentage of females and copepodites were found in the > 200 m in 1995 than either 1996 or 1997

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143 (15.9% vs. 13.6 and 13.6%) while Oithona spp. males showed an increasing proportion of their populations found in the larger size category year to year, amounting to 15.7, 22.0 and 29.7% for 1995, 1996 and 1 997, respectively. Seasonal differences were noted in Oithona spp. (females and copepodites) size distributions, with a higher proportion of the population found in the > 200 m size fraction in winter and summer (both 15.8%) than spring or fall correspond ing to 11.4 and 13.9%. Male Oithona spp showed a similar seasonal pattern but with even greater differences (winter and summer, 30 and 37%, respectively compared to spring and fall, 16 and 8%, respectively). Microsetella spp. (including copepodites) had an overall of 93% of its population passing through the 200 m screen. Annually, 1996 had a slight decrease in this proportion to 84.3% compared to 91.1 and 93.2% for both 1995 and 1997, while, seasonal analysis revealed spring and summer to have the lowes t percentage of Microsetella spp. population retained by the 200 m screen (< 1/3 of either winter or fall). This was likely due to fewer copepodites in winter and fall as well as a greater proportion of M. rosea in fall. These seasonal differences were st atistically significant (K W, p = 0.004, M.C., all p values < 0.05). When adults of the two component species of Microsetella were analyzed separately, different overall, annual and seasonal distributions among the 2 size fractions were noted. The larger species, Microsetella rosea, had an overall of 71% of its adult population found in the > 200 m size fraction while M. norvegica had only 2% in the larger size category. Annually, M. rosea had a stable distribution among years, varying by less than 2%,Whi le Microsetella norvegica had a trend of increasing proportions of adults found in the > 200 m size fraction form 1995 to 1997 (0.85 to 2.5%). Seasonal analysis showed significant differences. Microsetella rosea had the lowest fraction of the adult popula tion retained by the 200 m screen in summer (42%) compared to all other seasons (ranging from 71 to 83%) and this difference was statistically significant (K W, p = 0.05). Microsetella norvegica had a different seasonal pattern with a minimal proportion o f adults found in the larger size category in spring and the greatest in fall (0.61 vs. 3.3%, respectively). Both of these seasonal patterns of size distributions may have been due to the first peak in population being composed of smaller adults while the second peak generation had more favorable growing conditions leading to larger body sizes.

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144 Table 28 Percentage contribution of the >200 and 64 200 m size fractions to total abundance m 2 (0 150 m) of various non calanoid species for all Taylor tows analyzed (1995 1997) Species Size fraction 1995 1996 1997 All years Winters Springs Summer Falls Microsetella rosea > 200m 69.60% 69.89% 71.91% 70.59% 82.50% 71.98% 41.96% 71.06% 64 200 m 30.40% 30.11% 28.09% 29.41% 17.50% 28.02% 58.04% 28.94% Microsetella norvegica > 200m 0.85% 1.57% 2.48% 1.72 % 1.73% 0.61% 1.72% 3.30% 64 200 m 99.15% 98.43% 97.52% 98.28% 98.39% 99.39% 98.28% 96.70% *Total Microsetella spp. > 200m 6.25% 8.22% 6.65% 7.06% 9.96% 2.44% 3.20% 11.58% 64 200 m 93.75% 91.78% 93.35% 92.94% 90.04% 97.56% 96.80% 88.42% > 200m 64.24% 70.28% 72.62% 69.51% 73.04% 72.59% 55.87% 70.26% 64 200 m 35.76% 29.72% 27.38% 30.49% 26.96% 27.41% 44.13% 29.74% Mixed Oncaea spp. > 200m 13.84% 31.27% 22.54% 23.04% 28.12% 13.27% 26.37% 24.69% 64 200 m 86.16% 68.73% 77.46% 76.96% 71.88% 86.73% 73.63% 75.31% > 200m 36.66% 59.45% 48.08% 48.06% 47.70% 49.35% 48.65% 46.23% 64 200 m 63.34% 40.55% 51.92% 51.94% 52.30% 50.65% 51.35% 53.77% > 200m 5.10% 6.54% 3.27% 4.77% 4.92% 0.24% 9.01% 7.38% 64 200 m 94.90% 93.46% 96.73% 95.23% 95.08% 99.76% 90.99% 92.62% Oncaea > 200m 0.00% 0.11% 0.00% 0.04% 0.00% 0.00% 0.00% 0.18% 64 200 m 100.00% 99.89% 100.00% 99.96% 100.00% 100.00% 100.00% 99.82% Oncaea copepodites > 200m 1.33% 1.27% 1.06% 1.12% 1.46% 0.75% 1.55% 1.10% 64 200 m 98.67% 98.73% 98.94% 98.79% 98.54% 99.25% 98.45% 98.90% *Total Oncaea spp. > 200m 3.88% 4.90% 4.25% 4.36% 3.60% 3.83% 5.62% 5.47% 64 200 m 96.12% 95.10% 95.75% 95.64% 96.40% 96.17% 94.38% 94.53% > 200m 91.11% 84.31% 93.21% 89.52% 100.00% 87.48% 91.11% 70.35% 64 200 m 8.89% 15.69% 6.79% 10.48% 0.00% 12.52% 8.89% 29.65%

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145 Table 28 (continued) Species Size fraction 1995 1996 1997 All years Winters Springs Summer Falls Corycaeid copepodites > 200m 18.29% 15.46% 18.15% 17.27% 18.66% 12.57% 15.55% 23.07% 64 200 m 81.71% 84.54% 81.85% 82.73% 81.34% 87.43% 84.45% 76.93% > 200m 15.92% 13.58% 13.55% 14.21% 15.82% 11.42% 15.82% 13.85% 64 200 m 84.08% 86.42% 86.45% 85.79% 84.18% 88.58% 84.18% 86.15% > 200m 15.73% 22.01% 29.65% 23.23% 30.40% 16.30% 36.61% 8.37% 64 200 m 84.27% 77.99% 70.35% 76.77% 69.60% 83.70% 63.39% 91.63% > 200m 15.56% 28.57% 44.52% 33.45% 33.33% 33.42% 0.00% 44.76% 64 200 m 84.44% 71.43% 55.48% 66.55% 66.67% 66.58% 100.00% 55.24% Total non calanoid copepods > 200m 8.68% 10.11% 9.21% 9.36% 8.91% 7.58% 10.61% 11.67% 64 200 m 91.32% 89.89% 90.79% 90.64% 91.09% 92.42% 89.39% 88.33% Larvaceans ( <=2mm) > 200m 18.05% 11.61% 11.20% 13.24% 16.77% 11.43% 9.36% 12.58% 64 200 m 81.95% 88.39% 88.80% 86.76% 83.23% 88.57% 90.64% 87.42% Includes copepodites

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146 The last group of non calanoids analyzed, Corycaeidae copepodites, had an overall of 17.3% of the population present in the > 200 m size fraction with lowest annual proportions in 1996 (15.5%) compared to 18.3 and 18.2% for 1995 and 1997, respectively. Seasonally, the highest percentage of Coryca eidae copepodites found in the large size fraction was in fall (23%) and lowest in spring (12.6%). Discussion Comparisons with previous studies in the BATS vicinity There are very few published studies that measured the biomass and even fewer that re ported the abundance of microzooplankton in the vicinity of the BATS Station. One study that described both biomass and abundance of < 200 m zooplankton was that of Bttger (1982). She examined 10 samples from 10 stations in the Sargasso Sea close to the BATS site (between ~ biomass (0 200 m), using a 100 m mesh net in late March and early April. Overall biomass was 1,311mg dwt m 2 (assuming a ratio of dry weight to wet weight of 19% from Madin et al. 2001), as opposed to an overall average of 756 mg dwt m 2 for 33 > 200 m net samples and 209 mg dwt m 2 for 64 200 m fractions (965 mg dwt m 2 for zooplankton > 64 m) for tows condu cted in March (1995 to 1999). In addition to biomass, abundance from four 55 m net tows from 2 stations near BATS (~ 3 (excluding protozoans) was found. This compares to an average of 8,195 animals m 3 for all zooplankton (including tintinids) for all 36 Taylor tows and 9,842 individuals m 3 for March and early April samples (64 200 m size fraction). To correct for the exclusion of > 200 m zooplankt on t he average numbers counted for the non calanoid copepods and larvaceans > 200 m were added (222 and 264 animals m 3 for overall and March early April tows, respectively). Using the results of Deevey (1971), in which she found non calanoid copepods to make up 40.5% of overall copepod abundance, would increase the estimates for > 200 m zooplankton numbers to 481 and 567 animals m 3 for overall and March early April tows, respectively. Thus, the abundance of overall and March early April Taylor > 64 m zoopl ankton samples would be 8,676 and 10,409, respectively.

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147 Further comparisons can be made for adult copepods and copepodite stages counted as one category by Bttger (1982) as well as copepod nauplii, larvaceans, and mollusks. The 64 200 m size fractions o verall and March early April abundances were 2,616 and 3,422 individuals m 3 respectively, for combined copepod adults and copepodites. Nauplii of copepods averaged 4,934 and 5,723 animals m 3 for overall and March early April Taylor 64 200 m samples, r espectively. The previous results compare reasonably well to the estimates of Bttger (1982) of 1,750 for copepod adults and copepodites (range = 850 5,000) and 3,600 individuals m 3 for nauplii (range = 1,500 7,900). Other groups enumerated by Bttger (19 82) included larvaceans and mollusks. They averaged 140 (range = 28 1,200) and 110 animals m 3 (range = 21 180), respectively. Her numbers compared well to overall and March early April respective averages of 310 and 365 for larvaceans and 44 and 48 indivi duals m 3 for mollusks of the BATS 64 200 m samples. In more recent studies, Roman et al. (1993 and 1995) found total biomass (converted from their carbon to dry weights assuming a C : dwt of 36% from Madin et al., 2001 and integrated to 150 m ) to be similar in spring and summer for the > 64 m zooplankton (1,644 and 1,586 mg dwt m 2 respectively). However, they noted a marked seasonal difference in the distribution of biomass among macro (> 200 m) and mesozooplankton (64 200 m), with t he former com prising 75% of > 64 m dry weight in March/April and only 30% in August. The > 200 m fraction biomass estimates of Roman et al. (1,233 mg dwt m 2 ) are well above the average at BATS (1995 1997) for pooled samples from March early April (531 mg dwt m 2 ) bu t were within the cruise averaged range found at BATS from 1994 1998 (140 1,582 mg dwt m 2 ). However, their August average of 467 mg dwt m 2 was identical to that of the BATS August mean of 456 dwt m 2 The discrepancy of the spring estimates was lessened by the addition of biomass from the 64 200 m size fractions of the Taylor tows (209 and 159 mg dwt m 2 for March early April and August, respectively). However, it was still substantially less than that measured by Roman et al. for the 64 200 m size fr action (306 and 839 mg dwt m 2 ) during the same times of year. The inconsistency between estimates of > 64 m biomass of the present study and those of Roman et al. may be due to several factors which are not necessarily mutually exclusive. The first may b e that the present study underestimated biomass in the 64 200 m due to the inclusion of only copepods and their larvae. Also, the methodology used to calculate the dry weight of individual animals may have contributed to an underestimation of biomass but it likely

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148 would not have been enough to account for the large difference found. Thus, it is likely that the differences are due to the patchy nature of zooplankton abundance due t o factors discussed in chapter 2 (e.g. mesoscale eddies, storms and internal waves). As a way of checking the reasonableness of the biomass estimates made for the 64 200 m size fraction, all size fractions of BATS > 64 m biomass (1995 1997) were compared (Table 29 ) The uniformity of biomass within each zooplankton size categor y (i.e. caught between 2 screens one roughly double the pore size of the other) was striking. The results were consistent with those of Madin et al. (2001) at BATS and Landry et al. (2001) at the HOT site. The present results are consistent with the genera l pattern of pelagic systems to have similar amounts of particulate matter within logarithmically equal size ranges (Sheldon et al., 1972) or slightly decreasing biomass with increasing size of the animals within a particular size category (Platt and Denma n, 1978; Rodriguez and Mullin, 1986a, 1986b). The size fractions compared here encompass those created by sieving through a series of screens with the following mesh sizes: 5, 2, 1, 0.5, 0.2 and 0.064 mm. These encompass the following ratios of larger to smaller pore size: 2.5, 2, 2, 2.5 and 3.2. It would be expected that the 64 200 m size fractions should have just under twice the biomass as that retained in the other categories. Looking at results of the comparisons in Table 29 (disregarding the > 5 mm category that was likely not sampled adequately by the 1 m 2 200 m net used) confirms the theory and observations of other investigators at BATS and HOT with an overall of 44% of the total biomass of the > 200 m net samples, very close to double the aver age of each other size fraction. Thus, it appears that the biomass estimates of the present study for the 64 200 m size categories appear to be reasonable. The oncaeid microcopepod community at BATS Eleven identified oncaeid species were found at BATS in the upper 150 m and at least one unidentified one compared to deep (~ 1000 m) fine mesh samples taken in the Mediterranean, Red and Arabian Seas with a total of 28, 26 and 69 species. It is almost certain that the number of species found at BATS would b e considerably higher if depths deeper than 150 m were sampled with the fine mesh nets as

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149 Table 2 9 Cruise averaged total and size fractionated b iomass (mg dry weight m 2 0 150 m) form BATS and Taylor tows (1995 1997) Net system >5mm (% total) 2 5mm (% total) 1 2mm (% total) 0.5 1mm (% total) 0.2 0.5mm (% total) Total >0.2mm 64 200 m (%BATS) ALL BATS 200 m tows (C.V.) 34 (59%) 8.6% 90 (54%) 22.8% 90 (57%) 22.8% 99 (39%) 25.1% 81 (56%) 20.6% 394 (41%) 177 (42%) 44.9% Night BATS 200 m tows (C.V.) 44 (68%) 9.6% 123 (55%) 26.7% 110 (52%) 23.9% 105 (47%) 22.8% 80 (33%) 17.4% 460 (42%) 177 (42%) 38.5% Day BATS 200 m tows (C.V.) 23 (80%) 7.0% 59 (68%) 18.0% 70 (77%) 21.3% 94 (43%) 28.7% 84 (39%) 25.6% 328 (47%) 177 (42%) 54.0% Closets BATS To Taylor tows 35 (61%) 7.9% 121 (68%) 27.3% 106 (61%) 23.9% 105 (49%) 23.7% 76 (48%) 17.1% 444 (49%) 177 (42%) 39.9% Biomass from wet sieved preserved samples (64 200 m) and constitutes all copepods and their larvae only coefficient of variation is standard deviation / mean many species were found to be restricted to meso and bathypelagic depths (Bttger Schnack, 1990a, 1996a and b). In order to gain insight into how the o ncaeid m icrocopepod abundance patterns at BATS com pare with the few pub lished results, estimations of six species found at BATS were compared to findings from five other previous ly mentioned studies (Table 30 ). The comparison revealed higher abundance for the BATS area compared to most studies. However, w hen a species by species comparison was made some notable departures from the overall pattern emerged. For example, in the Central (winter and fall) and Northern (fall only) Red Sea, the larger sized species Triconia minuta and T. dentipes were found in si milar numbers as BATS (within a factor of 2), however, the smaller species were considerably lower compared to overall and comparable seasons (e.g. Spinoncaea ivlevi a factor of 5, O. zernovi a factor of 8, and especially O. vodjanitskii a factor of 42, l ower than at BATS). While the very small O. atlantica was so rare that it did not warrant quantitative analysis in the studies of Bttger Schnack (1990a and 1990b). A possible reason for this may have been the coarser net used to sample these copepods (100 vs. 55 m) that may have under sampled the smaller o ncaeid species. This could have been the cause of the lower abundances of the small species, since a later study (Bttger Schnack, 1995) conducted in the summer using 55 m nets revealed numbers more in line with averages from BATS. Reasons for the discrepancies, other than natural differences in productivity and hydrography, could have included either overestimation of BATS numbers, underestimations in the other studies or a

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150 combination of both. The possibility of ove restimations of the BATS micro o ncaeid numbers comes from the possibility of erroneous flowmeter reading s due to potential net clogging that would underestimate the volume of water filtered thus leading to ov erestimations of copepod abundance. Clogging of nets, while Table 30 Comparison between abundance (copepods m 2 ) of oncaeid microcopepods within the epipelagic (0 100) layer from the BATS region and previous studies BATS (1995 1999) (64 200 m) a A rabian Sea (spring, 1987) 55 m nets b Mediterranrean (winter, 1987) 55 m nets c, d Red Sea (1980 1981) 100 m nets e Red Sea and Gulf of Aden (Summer, 1987) 55 m nets Triconia minuta Winter (403) Spring (665) Summer (800) Fall (804) Overall (620) Not mentioned (37) Central (fall) (250) Central (winter) (550) Northern (fall) (610) G.A. 156 (night ) B.A. 300 S.S. 380 S.D. 300 C 1.56 x 10 3 N 1.72 x10 3 Triconia dentipes Winter (3.13 x 10 3 ) Spring (4.01 x 10 3 ) Summer (4.21 x 10 3 ) Fall (5.74 x 10 3 ) Overall (4.06 x 10 3 ) Oman coast (day ) (2.12 x 10 3 ) Central Arabian Sea (1.24 x 10 3 ) (1.08 x 10 3 ) Central (fall) (3.00 x 10 3 ) Central (winter) (2.70 x 10 3 ) Northern (fall) (3.00 x 10 3 ) G.A. 684 (night ) 1.44 x 10 3 (day ) B.A. 2.68 x 10 3 S.S. 2.22 x 10 3 S.D. 572 C 2.15 x 10 3 N 1.28 x 10 3 Oncaea zernovi Winter (25.97 x 10 3 ) Spring (27.15 x 10 3 ) Summer (13.14 x 10 3 ) Fall (15.38 x 10 3 ) Overall (22.10 x 10 3 ) Oman coast day (3.32 x 10 3 ) Central Arabian Sea (4.80 x10 3 ) (9.60 x 10 3 ) Central (fall) (2.30 x 10 3 ) Central (winter) (2.60 x 10 3 ) Northern (fall) (3.00 x 10 3 ) G.A. 17.4 x 10 3 (night ) 8.80 x 10 3 (day ) B.A. 19.20 x 10 3 S.S. 18.00 x 10 3 S.D. 16.40 x 10 3 C 8.00 x 10 3 N 2.56 x 10 3 Spinoncaea ivlevi Winter (13.64 x 10 3 ) Spring (14.39 x 10 3 ) Summer (12.23 x 10 3 ) Fall (20.08 x 10 3 ) Overall (14.86 x 10 3 ) Oman coast day (none) Central Arabian Sea (exoskeletons only) (7.20 x 10 3 ) Central (fall) (3.50 x 10 3 ) Central (winter) (3.40 x 10 3 ) Northern (fall) (3.30 x 10 3 ) G.A. 5.60 x 10 3 (night ) 7.60 x 10 3 (day ) B.A. 8.80 x 10 3 S.S. 14.00 x 10 3 S.D. 9.60 x 10 3 C 31.60 x 10 3 N 22.40 x 10 3 Oncaea atlantica Winter (1.96 x 10 3 ) Spring (2.51 x 10 3 ) Summer (3.88 x 10 3 ) Fall (6.73 x 10 3 ) Overall (3.36 x 10 3 ) Oman coast day (1.28 x 10 3 ) Central Arabian Sea (136) Not mentioned Central (fall) (rare) Central (winter) (rare) Northern (fall) (rare) G.A. 92 B.A. 2.60 x 10 3 S.S. 2.52 x 10 3 S.D. 296 C 920 N 1.00 x 10 3 Oncaea vodjanitskii Winter (543) Spring (831) Summer (831) Fall (891) Overall (744) Oman coast (D) (256) Central Arabian Sea (exoskeletons only) (3.08 x 10 3 ) Central (fall) (100) Central (winter) (20) Northern (fall) (10) G.A. 112 B.A. 960 S.S. 1.20 x 10 3 S.D. 480 C 2.10 x 10 3 N 1.80 x 10 3 Abbreviations used: G.A= Gulf of Aden, B.A= Bab al Mandab, S.S= South Shallow, S.D= South Deep C= Central, N= North Oncaea a tlantica and O. vodjanitskii abundance from entire depth sampled (175 1050m) a Bttger Schnack (1996a) b Bttger Schnack (1996b) c Bttger Schnack (1990a) d Bttger Schnack (1990b) e Bttger Schnack (1995)

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151 said to be unnoticed from visual examination at the end of net tows, nonetheless, could have led to less than the 100% filtration efficiency assumed in the Bttger Schnack studies. For example, if the nets filtered water at an efficiency of 80% then abund ance would be underestimated by 25% and a further drop to 67% efficiency would lead to an underestimation by 50%. Knowledge of the zoogeography of the six species of micro o ncaeid copepods discussed above is patchy at best, particularly for those species less than 0.5 mm in length ( Oncaea zernovi O. atlantica O. vodjanitskii and Spinoncaea ivlevi ). However, O. zernovi and S. ivlevi were the subjects of efforts to gather worl dw ide records of their presence as well as any quantitative data on their numbers and vertical distribution (Bttger Schnack 2002 and 2003). Oncaea zernovi is likely a ubiquitous and abundant copepod of the epi and upper mesopelagic pical and subtropical oceans (Bttger Schnack 2002). This species has been reported from the northeastern Atlantic upwelling off Africa, both sides of the Pacific off northern California and Japan as well as the eastern Indian Ocean off northwest Australi a (Bttger Schnack, 2002). It has also been reported off the coast of Brazil and Argentina in the Atlantic ( Razouls et al., 2008) in addition to the previously mentioned specific areas of the Arabian and Red Seas and the eastern Mediterranean. The next s pecies, Spinoncaea ivlevi was first described, as was Oncaea zernovi from the Adriatic Sea (Shmeleva, 1969) and has previously been reported to inhabit the Atlantic in the southern tropical and subtropical areas off North Africa (Malt, 1982). It was subs equently quantified in the eastern Mediterranean (Bttger Schnack, 1996b) and was found in great numbers in the Red Sea, although, no live specimens were sampled in the Arabian Sea (Bttger Schnack, 1990a, 1990b, and 1996a). However, S. ivlevi was confirme d as present in sample s from both the eastern equatorial as well as the southwest Indian Ocean in addition to the north east and north west Pacific Ocean (Bttger Schnack, 2003). T he two smallest species of micro o ncaeids Oncaea atlantica and O. vodjanits kii were found in lower numbers compared to O. zernovi and S. ivlevi and their zoogeography is more poorly known. As the name implies, O. atlantica was first described from the southwestern Atlantic (Shmeleva, 1967) and has been confirmed in the Red Sea as well as the Arabian Sea (Boxshall and Bttger, 1987). It was not

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152 mentioned in any of the previously mentioned fine mesh studies in the Mediterranean but was noted as present in the eastern and far west Mediterranean by Razouls et al. (2008). Oncaea vodjan itskii on the other hand was first described from samples taken in the Adriatic Sea (Shmeleva and Dlalo, 1965). This very small species has also been reported from the eastern Mediterranean, Arabian and Red Seas (Bttger Schnack, 1990a, 1990b, 1996a and and Malt (1985) although the location was not specified. All four of these very small (< 0.5 mm) copepod species ( Spin oncaea ivlevi, Oncaea zernovi, Oncaea atlantica and O. vodjanitskii ) un doubtedly have a much wider range but due to the limited number of studies employing fine mesh nets (< 0.1 mm) they are rarely sampled at all let alone quantitatively. As far as the author knows, of the six micro o ncaeid s found in the present study, only T riconia minuta and T. dentipes were previously recorded in the Sargasso Sea (Deevey, 1971). In fact the previous two species have been reported from all major ocean basins in tropical and subtropical regions and T. minuta has also been reported in the Subarctic Atlantic and Pacific as well as the Arctic Ocean, while T. dentipes has only been reported in the subarctic Pacific ( Razouls et al., 2008). Thus, the present study is the first confirmed documentation of Oncaea zern ovi O. atlantica O. vodjanitskii and S. ivlevi in the Sargasso Sea. Assumptions used in estimating role of Microsetella spp. in at BATS Previous studies have noted the presence of Microsetella norvegica attached to marine snow particles, often orders of magnitude more enriched within the aggregates than in the surrounding seawater (Alldredge, 1972; Ohtsuka et al ., 1993; Steinberg et al., 1994; Dagg and Gr een, 1997). As is the case for miraciid harp acticoids discussed in chapter 3 Microsetella spp. see ms to be a pseudopelagic genus ill suited for life in the open ocean but one that has adapted by associating itself with particles drifting in the water column. Microsetella norvegica seems to be most efficient feeding on surface attached particles and was found to feed inefficiently from suspension (Koski et al., 2005) The surface feeding preference was confirmed in experiments using diatoms attached to glass surfaces (Koski et al., 2005) and discarded

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153 larvacean houses (Koski et al., 2007). In both cases M. norvegica was observed to feed well on surface attached particles. The assumption that Microsetella spp. obtains all of its nutritional requirements from sinking aggregates may not be 100% correct. For example Uye and Onb (2002) stated that they did n ot observe Microsetella norvegica to be associated with aggregates at their eutrophic study area. However, several authors have noted that Microsetella norvegica association with discarded appendicularian houses increases from eutrophic and mesotrophic n eritic areas to more oligotrophic oceanic systems (Ohtsuka et al., 1993; Green and Dagg, 1997; Uye and Onb, 2002). Hence, the importance of marine snow aggregates to Microsetella spp. would likely be higher at low productivity oceanic regimes such as the BATS site. Another piece of circumstantial evidence comes from the vertical distribution of Microsetella norvegica that seems to concentrate at or just below the pycnocline (Maar et al, 2006). Aggregates of marine snow also tend to accumulate at the pycnoc line due to slowed sinking rates at density discontinuity layers (MacIntyre et al., 1995; Alldredge et al., 2002). In addition, Maar et al. (2006) found a significant non linear correlation between M. norvegica abundance and house recycling. Moreover, the y found no significant relationship for any o f the seven copepod taxa they analyzed The second assumption made here, that larvacean house formation rate is a good representative of aggregate marine snow production in the photic zone is explored. Marine snow is formed by many processes, one of which is larvacean house production. Marine snow aggregates, define d here as particles > 0.5 enhanced physical aggregation of smaller particles (Alldredge and Silver, 1988). Appendicularian houses constitute a major proportion of marine snow, par ticularly during peak abundance, of the amount produced by other mechanisms and have been shown to compose nearly one quarter of all marine snow particle abundance (Alldredge, 1979). The importance of larvacean houses to total marine sn ow abundance should be more pronounced in regions where abundance and temperature are high and other sources of aggregates are less common. Larvaceans comprised ~ 8 % of total zooplankton numbers in 200 m net samples taken in a study by Deevey (1971) nea r BATS Therefore, larvaceans make up an important fraction of the total zooplankton abundance behind copepods (~ 70%) However, larvaceans have some of the highest growth

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154 rates of any metazoan group on earth and much of their production goes towards house construction (Hopcroft, 1998). Kirboe (2000) noted that the size of the aggregate was an important factor in their remineralization rates with larger particles containing more abundant and larger metazoan colonizers capable of more quickly consuming and breaking them up despite their shorter residence time in the photic zone. He found that the abundance of metazoan colonizers scales with the radius of the aggregate to the power 2.27 when compared to ambient water that may imply simple scavenging as the ma in encounter mechanism. However, another means must be employed since simple hydrodynamic encounter rates cannot account for such high enrichment of colonizing metazoans on marine snow particles. It has been suggested that Microsetella spp. likely utilizes chemical signals to remotely detect the plume of organic solutes left behind by sinking organic aggregates, thus vastly increasing their encounter rates (Kirboe and Thygesen 2001; Marr et al., 2006; Koski et al., 2007). Remote detection of aggregates by copepods would be especially important in more oligotrophic regions such as the Sargasso Sea. The modest amounts of aggregate consumption by Microsetella spp. should not be viewed as the only way in which it can affect aggregates. Physical disruption of large particles of marine snow is likely an important means by which Microsetella spp. influence particle dynamics at the BATS site. When large aggregates (e.g. discarded larvacean houses) are physically disrupted, the resulting fragments will sink more sl owly (i.e. spend more time in surface waters at higher temperatures) and along with increased surface area will allow a much higher rate bacterial degradation. This type of physical disruption was suggested by Steinberg et al. (1997) as a means of increasi ng the rate of remineralization of mesopelagic giant larvacean houses by metazoan colonizers that included Microsetella spp. and Oncaea spp. among others. More recently, Goldthwait et al. (2004) actually proved that physical contact by Euphausia pacifica was an important mechanism of altering marine snow size structure without loss of POC total mass. Physical disruption of large marine snow aggregates was one of the means proposed by Karl et al. (1988) to explain the exponential decline with depth below t he mixed layer of POC demonstrated by Martin et al. (1987). Thus, copepod species with an affinity for marine snow aggregates can significantly modify the quantity of POC reaching deeper layers of the open ocean.

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155 Summary and conclusions As the results of the present study have shown, micro metazoans retained by 64 m meshes but extruded through 200 m nets dominate abundance and form a substantial portion of the zooplankton biomass sampled by standard zooplankton nets (i.e. > 200 m). Moreover, they con tribute to rate processes at BATS disproportionally to their biomass N recycling and grazing rates (as C demand) are on a par with the mesozooplankton. Furthermore, it was found that the current zooplankton sampling protocol used at BATS missed the vast ma jority of Microsetella norvegica a very abundant species in the 64 200 m but very rare in the > 200 m fractions (< 2% retained by 200 m screen) and an entire community of micro oncaeid copepods, with 1 species severely under sampled (< 5% caught by the 200 m net) and four identified and one unidentified species never observed in any of the 131 samples examined of the 200 m net tows. The micro copepods likely play an important role in the remineralization of organic aggregates at BATS, with an estima ted 8 and 10% of larvacean house production consumed daily in the upper 150 m of the water column by Microsetella spp and oncaeid copepods in this size category. Finally, the four identified species of micro oncaeids in the present investigation ( Oncaea z ernovi Spinoncaea ivlevi O. atlantica and O. vodjanitskii ) were the first recordings of their presence in the Sargasso Sea. Due to their importance in trophic transfer and elemental cycling every effort should be made to properly sample the micro metazoans at BATS. More effective microzooplankton (64 200 m) sampling could be achieved by including at least 1 day and 1night vertical tow in the upper 200 m of the water column using fine mesh nets along with a few deep tows (upper 2,000 m) taken during each season employing multiple nets. Such as scheme would produce new insights on the vertical distribution of micro copepods and would likely lead to the discovery of new species of the very rarely sampled micro copepods of the meso and bathypelag ic realm. Future stable isotopic study of the micro oncaeids and Microsetella spp could help discern the true trophic position of these suspected detritivores, potentially adding a great deal to our knowledge of the fate of sinking elements, particularly carbon, at BATS.

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156 Chapter Five Sex Ratios of Non Calanoid Copepods at BATS (1995 1999)

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157 Introduction In dioecious species, sex is determined either by genetic or by environmental factors, although neither of them decides sex exclusively (Bull, 1983). In copepods the exact mechanism of sex determination is not known for certain, though there is a consensu s that it is largely under genetic control with room for influence by various environmental factors (Fleminger, 1985). The combination of genetic and environmental mechanisms for determining sex is known as a polygenetic system, where members of a species possess genes capable of expressing either the male or female phenotype depending on external cues (Bull, 1983). Other investigators have claimed chromosomal control of gender with heterogamety of sex chromosomes found in males of several families of calan oid copepods including Centropagidae, Pontellidae, Acartiidae and Tortanidae all members of the super family Centropagoidea (Fleminger, 1985 and references therein). As detailed by Charnov and Bull (1977), environmental sex determination (ESD) is selected for when the progeny of a species enter a heterogeneous or patchy environment that confers differential survivability of the sexes, which makes fixed genetic sex determination (GSD) less favorable. Examples of environmental factors influencing sex determi nation include competition for mates, availability of resources with differing importance to each sex as well as gender specific mortality due to predation. Those reasons, along with the inability of parents and offspring to choose the best sex specific pa tch render ESD a system that will lead to better fitness over GSD. Examples of ESD in free living pelagic copepods include those of Fleminger (1985), Svenson and Tande (1999) and Irigoien et al. (2000). All of those studies showed changes in sex ratio duri ng development in calanid copepods due to external factors. Biological oceanographers usually emphasize food availability, physical, and chemical parameters such as temperature and salinity, and the presence of predators when studying population dynamics of copepods. However, there is one, sometimes overlooked, aspect of the biology of copepods that may be an important factor in shaping and maintaining observed population structure rates of fertilization. Copepods reproduce sexually with the male functioni ng as the active participant in 3 of the 5 steps of the mating process (Ohtsuka and Huys, 2001) namely; 1) mate recognition 2) capture and physical control of the

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158 female 3) attachment of spermatophore 4) fertilization and release of eggs by the female and 5) removal of the spent spermatophore by the female. Mate encounter is a particularly daunting task given the 3 dimensional nature of the pelagic environment as well as the low densities of many copepod populations in oligotrophic oceanic environments. For the vast majority of pelagic copepods the solution is to use chemical cues (gynopheromones) where chance encounters would never suffice. The pheromones are emitted by receptive females and can be detected by the males in extraordinarily dilute concentrati ons (Katona, 1973; Boxshall and Huys, 1998; Kiorboe et al., 2005; Kiorboe, 2007). Male copepods sense these gynopheromones through chemosensory structures on their antennae known as aesthetascs. The structures are more numerous in males, especially in oce anic species (Boxshall and Huys, 1998), and are mainly confined to males of more recently evolved calanoid superfamilies. They seem to be an adaptation to life in the open ocean (Huys and Boxshall, 1991). Moreover, there is speculation that males may use integumental organs to locate female pheromone trails (Fleminger, 1973; Fleminger and Hulsemann 1977). However, according to Ohtsuka and Huys (2001) no direct neurophysiological evidence is available to conclusively prove the gynopheromone system of mate a ttraction. In addition to chemical signaling, vision may play a role in mate recognition and location. This has been documented in the family Pontellidae (Ohtsuka and Huys, 2001) but could be involved in the non calanoid families Sapphirinidae and Corycae idae, each containing species with well developed lenticular eyes similar to members of the family Pontellidae. Iridescence in Sapphirina species may be involved in mate recognition (Chae and Nishida, 1995). In addition, some species may utilize biolumines cence in mate recognition e.g. Triconi a conifera (Herring et al., 1993). Males of families whose constituents lack double aesthetacs (members of the superfamily Centropagoidea) may employ mechanosensory means to find females. Females of these families hav e pronounced sexually dimorphic posterior prosomal and urosomal extensions that may aid in creating species specific hydromechanical signals (Boxshall and Huys, 1998). Females of the super family do not posses seminal receptacles and must mate repeatedly ( once for each batch of eggs produced). The fact that these species do not seem to possess a chemical signaling system and females cannot store sperm for multiple spawning is likely the reason they have a near 1:1 sex ratio. It is also interesting to recall that gender in these families is thought to be mainly genetically determined.

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159 In addition to the mate searching capacity of males mate handling time and spermatophore production capability may limit fertilization rates of female copepods (Ianora et al., 1989; Hopkins, 1982). This may result in not all adult females being fertilized (Hopkins, 1982; Williamson and Butler, 1987) and limited fertilization caused by too few mate encounters (Stephens et al., 1999; Kirboe, 2006). In fact the percentage of fertilized females is directly related to the abundance of males (Hopkins, 1982; Williamson and Butler, 1987). Thus, mating capacity and the implicitly inc luded sex ratio are important parameters in copepod population dynamics and persistence in the ocean. There are a good number of field observations of copepod sex ratios; however, the vast majority of them deal with calanoids, with only a small percentage focusing on the non calanoid groups (Kirboe, 2006; Hirst and Kirboe, 2002). The following study will help build the record of non calanoid sex ratios observed in the field. Materials and M ethods Sample collection and analysis Samples used to study the sex ratios of both the > 200 m net and 64 200 m size fractions of the 20 and 35 m net systems deployed at BATS were collected and processed as described previously. Almost all adult species identified in the present study were separated into male an d female categories. The only species that were not divided into sex categories were Microsetella rosea and M. norvegica due to the difficulty of seeing the sexual characteristics. Additionally, Oithona spp were divided into adult males and females plus c opepodites, and the category of mixed Oncaea males was determined to be a mixture of three species ( O. media O. scottodicarloi and O. mediterranea ). Finally, there were a number of species that were represented by only females (the reverse was never the c ase). Those included Ratania flava Vettoria granulosa Mormonilla minor Pacos punctatum and Triconia minuta A total of 28 species were separated into sexes and their ratios analyzed for overall, annual and seasonal patterns. The analysis included keepi ng track of the total number of tows that actually contained the species (valid

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160 counts). An arbitrary cut off of 20 valid counts was imposed. Species that fell below this number were removed from further consideration. All the species considered in the Ta ylor (64 200 m) size fraction were present in sufficient samples for meaningful analysis (i.e. > 20). Finally, sex ratios were calculated and presented as the percentage that each sex contributed to the total abundance of adults in each sample except in t he case of Oithona which included copepodites in the female category. Results BATS 200 m net non calanoid sex ratios Overall sex ratios revealed different patterns for different groups and species. Pooling sex ratio results from all samples analyzed (n = 131) for all species within major families revealed an overall ratio in the family Sapphirinidae of 69% females and 31% males. The ratio changed slightly to 66% females and 34% males for the family Corycaeidae and 68 % females and 32% males for Oncaeid ae. Major deviations from the pattern above began with the family Lubbokiidae, with a ratio heavily skewed towards females (92%). The last major family, Oithonidae, had a sex ratio that was nearly 100% females. Over the entire data set of 131 tows only 0.2 1% of total Oithona spp were males, however, the counts of females included copepodites and this undoubtedly exaggerated their numbers considerably. The two remaining families, Clytemnestridae and Pontoeciellidae, were less common but abundant enough to w arrant analysis. They contained more females on average with 76 and 84%, for Clytemnestra scute llta and Pontoecielia abyssicola respectively. Finally, miraciid copepods had an overall female and male ratio of 69 and 31% of total adult abundance at BATS. The overall sex ratio patterns of the various families of non calanoid copepods at BATS masked differences among their constituent genera and also for the various species within them. Out of a total of seven species from the family Oncaeidae at BATS, five were analyzed for sex ratio patterns with three species being lumped into one category ( O. media O. scottodicarloi and O. mediterranea ). The overall ratio for the three species group was 72% and 28% for females and males, respectively. Overall results of

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161 the other two species of Oncaeidae were 59% and 49% females for Oncaea venusta and Triconia conifera respectively. The genus Corycaeus contained 10 species that were analyzed for trends in sex ratios. The first group consisted of two species of the subgenus Corycaeus C. speciosus and C. clause which had an overall ratio of 44% and 46% females, respectively. The second subgenus, Agetus made up of three species, had an overall mean of 44%, 37% and 34% females for C. typicus C. limba tus and C. flaccus respectively. The three species of the third Corycaeus subgenus, Onychocorycaeus had 35%, 37% and 67% females for C. latus C. giesbrechtii and C. brehmi respectively. The two species of the last subgenus, Urocorycaeus had on average 36% and 5% females, correspondingly, for C. lautus and C. furcifer The latter was a rare species and thus the very low ratio of females may not paint a true picture of the actual situation at BATS. The two species of the genus Farranula on the other han d had very different ratios of males and females. Farranula gracilis had, on average, 39% females and 61% males while F. rostrata ha d 96% females and only 4% males. It was suspected that the males of may have been small enough to have been under sampled by the 200 m net used to sample the zooplankton at BATS. However, it was found that the 200 m screen retained nearly 90% of adult male F. rostrata. Hence, the low ratio was not a sampling artifact. The family Sapphirinidae was represented by six species t hat were present in at least 20 samples. The percentages of females and males were variable among the species analyzed. Sapphirina metallina had an overall mean of 58% females and 42% males while the other less abundant species of S. nigromaculata and S. s tellata (present in 27 and 23 samples, respectively) had, on average, 85% females and 15% males for both species. The two species of Copilia analyzed, C. quadrata and C. mediterranea had overall sex ratios corresponding to 88% and 62% females, however, due to the prior removal of the > 2 mm size fraction of zooplankton by wet sieving from many of the samples, the larger sized males may have been under sampled in the present study. The final species of Sapphirinidae analyzed for its sex ratio was Corissa parva This species had an overall mean of 63% females and 37% males. Miraciid harpacticoid copepods Macrosetella gracilis and Oculosetella gracilis ha d higher percentages of females (2.55 and 2.11, M. gracilis and O. gracilis respectively), while, Miraci a efferata

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162 and Distioculus minor had female to male ratios close r to parity (1.26 and 1.17, D. minor and M. efferata respectively). Annual and seasonal sex ratio data on non calanoid copepod species are listed in Tables 31 and 32 Non calanoid copepod ge nera and species that were present in at least 5 samples for any year or season were statistically analyzed (Kruskal Wallis test) for annual and seasonal trends in the relative amounts of females versus males at BATS. Overall, there were few statistically significant annual differences among the species analyzed. Three species showed statistically significant differences among years. Triconia conifera had the lowest percentage females and conversely highest proportion of males in 1995 compared to all other years and was statistically different from 1997 1999 (K W, p < 0.001). Corycaeus brehmi had the highest percentage of females in 1996 and lowest in 1999 (K W, p = 0.016) while Farranula rostrata had the lowest proportion of males in 1996 (K W, p = 0.029). Seasonal analysis of sex ratios revealed significant differences for several species. This was particularly evident for members of the family Oncaeidae Taken as a whole oncaeid copepods showed highly significant differences between seasons with winter and spring composed of more females than males (K W, p < 0.001). This trend was followed by the category termed mixed Oncaea ( O. media, O. scottodicarloi and O. mediterranea ). Oncaea venusta had a slightly different seasonal pattern with spring alone composed of a significantly lower percentage of females than winter or fall. Triconia conifera had consistent percentages of males and females for all s easons and were close to a 1: 1 ratio. The other genus to exhibit different proportions of males and females among seasons was Corycaeus As a whole this genus did not reveal any apparent seasonal male to female ratio differences. However, when individual species were analyzed, some demonstrated s easonal differences in their sex ratios. Among these were Corycaeus speciosus with females significantly less abundant than males in spring as compared to summer (K W, p = 0.016) and Corycaeus brehmi that had the highest proportion of females in fall and l owest in spring (K W, p = 0.035). The final species to show significant seasonal differences in its male to female ratio was Farranula rostrata that had the highest proportion of males in spri ng and lowest in fall (K W, p < 0.001).

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163 Table 31 Annual sex ratios expressed as percentage of total numbers of selected non calanoid species for 1995 1999 BATS 200 m (0 200 m) net samples Species 1995 *n 1996 n 1997 n 1998 n 1999 n Macrosetella gracilis 75% 25% 16 74% 24% 14 73% 27% 23 64% 36% 15 72% 28% 21 Oculosetella gracilis 74% 26% 13 51% 49% 9 65% 35% 23 77% 23% 11 70% 30% 19 Maracia efferata 10% 90% 4 45% 55% 7 83% 13% 6 70% 30% 5 58% 42% 8 Distioculus minor 50% 50% 13 50% 50% 8 68% 32% 13 70% 30% 10 36% 64% 15 Clytemnestra scutellta 76% 24% 16 97% 3% 11 76% 24% 15 58% 42% 12 73% 27% 14 Sapphirina metallina 51% 49% 17 53% 47% 15 61% 39% 27 63% 37% 22 61% 39% 17 S. nigromaculata 95% 5% 5 89% 11% 8 80% 20% 5 60% 40% 5 100% 0% 4 S. stellata none none 0 56% 44% 3 96% 4% 6 89% 11% 7 83% 17% 7 Copilia quadrata 93% 7% 11 90% 10% 8 85% 15% 13 86% 14% 7 86% 14% 6 Copilia mediterranea 63% 37% 12 66% 34% 16 60% 40% 20 72% 28% 16 49% 51% 13 Lubbokia squillimana 90% 10% 23 90% 10% 22 93% 7% 30 93% 7% 25 92% 8% 26 Oncaea spp. 73% 27% 25 75% 25% 24 70% 30% 30 72% 28% 25 71% 29% 27 Oncaea venusta 62% 38% 22 55% 45% 23 54% 46% 29 58% 42% 20 68% 32% 16 Oncaea conifera 35% 65% 23 45% 55% 24 51% 49% 28 56% 44% 56% 56% 44% 24 Corycaeus speciosus 53% 47% 12 52% 48% 11 46% 54% 16 44% 56% 10 30% 70% 17 Corycaeus clausi 48% 52% 20 43% 57% 17 44% 56% 27 58% 42% 21 38% 62% 21 Corycaeus typicus 46% 54% 24 39% 61% 21 45% 55% 29 45% 55% 24 42% 58% 27

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164 Table 31 (continued) Species 1995 *n 1996 n 1997 n 1998 n 1999 n Corycaeus limbatus 30% 70% 23 41% 59% 22 38% 62% 28 36% 64% 25 41% 59% 27 Corycaeus flaccus 30% 70% 24 45% 55% 21 35% 65% 26 23% 77% 22 38% 62% 25 Corycaeus latus 37% 63% 10 26% 74% 11 36% 64% 14 34% 66% 9 40% 60% 15 Corycaeus lautus 50% 50% 8 38% 62% 12 27% 73% 19 41% 59% 13 34% 66% 19 Corycaeus furcifer 0% 100% 1 0% 100% 2 6% 94% 9 0% 100% 5 8% 92% 12 Corycaeus giesbrechtii 42% 58% 19 36% 56% 19 44% 56% 26 36% 64% 24 31% 69% 26 Corycaeus brehmi 65% 35% 22 88% 12% 16 68% 32% 21 68% 32% 24 53% 47% 21 Farranula gracilis 39% 61% 20 36% 64% 17 41% 59% 29 39% 61% 19 37% 63% 27 Farranula rostrata 93% 7% 24 98% 2% 24 97% 3% 30 96% 4% 25 93% 7% 27 Oithona spp. 99.72% 0.28% 25 99.91% 0.09% 24 99.76% 0.24% 30 99.78% 0.22% 25 99.81% 0.19% 27 Corissa parva 57% 43% 13 41% 59% 11 60% 40% 17 79% 21% 17 72% 28% 13 *n= number of samples that actually contained the species within the year O. media, O. scottodicarloi, and

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165 Table 32 Seasonal sex ratios expressed as percentage of total numbers of selected non calanoid species for 1995 1999 BATS 200 m net samples (0 200 m) Species Winters *n Springs n Summers n Falls n Macrosetella gracilis 67% 33% 30 77% 23% 17 73% 27% 14 73% 27% 28 Oculosetella gracilis 77% 23% 27 59% 41% 19 45% 55% 10 76% 24% 19 Maracia efferata 67% 33% 7 50% 50% 2 63% 37% 7 48% 52% 14 Distioculus minor 52% 48% 19 62% 38% 14 50% 50% 8 51% 49% 18 Clytemnestra scutellta 76% 24% 21 75% 25% 17 68% 32% 13 82% 18% 17 Sapphirina metallina 61% 39% 22 56% 44% 29 60% 40% 23 58% 42% 24 S. nigromaculata 50% 50% 2 90% 10% 7 84% 16% 8 88% 12% 10 S. stellata 83% 17% 4 75% 25% 6 92% 8% 4 89% 11% 9 Copilia quadrata 86% 14% 7 89% 11% 14 92% 8% 16 81% 19% 8 Copilia mediterranea 74% 26% 20 54% 46% 27 56% 44% 13 67% 33% 17 Lubbokia squillimana 91% 9% 31 91% 9% 37 88% 12% 29 96% 4% 29 Oncaea spp. 75% 25% 34 80% 20% 39 67% 33% 29 62% 38% 29 Oncaea venusta 69% 31% 28 50% 50% 39 54% 46% 25 69% 31% 18 Oncaea conifera 52% 48% 29 48% 52% 37 49% 51% 29 46% 54% 29 Corycaeus speciosus 33% 67% 9 30% 70% 9 64% 36% 19 39% 61% 29 Corycaeus clausi 40% 60% 21 45% 55% 33 44% 56% 27 55% 45% 25 Corycaeus typicus 45% 55% 29 46% 54% 38 43% 57% 29 40% 60% 29

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166 Table 32 (continued) Species Winters *n Springs n Summers n Falls n Corycaeus limbatus 42% 58% 30 36% 64% 38 38% 62% 29 32% 68% 28 Corycaeus flaccus 39% 61% 27 36% 64% 35 33% 67% 27 29% 71% 29 Corycaeus latus 25% 75% 6 51% 49% 5 29% 71% 23 40% 60% 25 Corycaeus lautus 18% 82% 11 39% 61% 23 50% 50% 17 30% 70% 20 Corycaeus furcifer 13% 88% 8 0% 100% 2 5% 95% 11 0% 100% 8 Corycaeus giesbrechtii 44% 56% 27 35% 65% 34 33% 67% 27 37% 63% 26 Corycaeus brehmi 66% 34% 20 62% 38% 38 66% 34% 26 82% 18% 20 Farranula gracilis 35% 65% 26 36% 64% 30 41% 59% 27 42% 58% 29 Farranula rostrata 96% 4% 34 94% 6% 39 95% 5% 29 98% 2% 28 Oithona spp. 99.86% 0.14% 34 99.88% 0.12% 39 99.64% 0.36% 29 99.76% 0.24% 29 Corissa parva 59% 41% 13 61% 39% 18 80% 20% 18 54% 46% 22 *(n) = number of samples that actually contained the species within the pooled season

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167 Taylor (64 200 m) non calanoid copepod sex ratios Overall, micro oncaeid species had a near 1:1 ratio of females to males (range = 0.81 to 1.35) with the notable exception of O. vodjanitskii that had a much higher proportion of females (> 6: 1). Oithona spp. on the whole had an extreme female to male ratio of over 46 to 1. Howe ver, it must be noted that the female counts included copepodite stages while the male abundance was strictly for adults. This likely exaggerated the ratio. This problem was mitigated by using abundance data of Paffenhffer and Mazzocchi (2003) gathered fr om 64 m nets taken at the BATS study site. Results of their study showed the percentage of copepodite stages to be approximately 90% of total Oithona spp numbers from the upper 100m of the water column both day and night. Therefore, to correct the data o f the present study, Oithona spp female abundance was multiplied by 0.1 to arrive at an overall ratio of 4.6 females for every male, a result that was in agreement with that found by Paffenhffer and Mazzocchi (2003). While annual differences in sex ratio s were noted among some of the species analyzed only those of Triconia dentipes and Oncaea zernovi were statistically significant. Triconia dentipes had fewer females in 1996 than 1995 and 1996 (K W, p = 0.041; M.C., p = 0.039, 1996 vs. 1997) while Oncaea zernovi had more females in 1996 (K W, p = 0.024; M.C., p = 0.031, 1996 vs. 1995). Seasonal analysis did not reveal any general trends in sex ratio variability. Some species had higher proportions of females in winter and fall vs. spring and summer (e.g. Spinoncaea ivlevi ) while others had peak percentages of females in spring and summer (e.g. Oncaea atlantica ) and none of the seasonal trends observed were statistically significant ( Table 33 )

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168 Table 33 Sex ratios expressed as percentage of total numbers of selected non calanoid species for all Taylor tows (64 200 m size fractions 0 150 m ) analyzed (1995 1997) Species 1995 1996 1997 Winters Springs Summers Falls Triconia dentipes 55% 45% 40% 60% 61% 39% 51% 49% 53% 47% 56% 44% 54% 46% Spinoncaea ivlevi 52% 48% 39% 61% 44% 56% 49% 51% 41% 59% 41% 59% 46% 54% Onacea atlantica 54% 46% 73% 27% 50% 50% 56% 44% 58% 42% 59% 41% 57% 43% Onceae zernovi / bispinosa 47% 53% 58% 42% 60% 40% 51% 49% 55% 45% 62% 38% 59% 41% Oncaea vodjanitskii 79% 21% 88% 13% 92% 8% 79% 21% 96% 4% 92% 8% 79% 21% 7 of 10 7 of 12 9 of 14 7 of 13 7 of 10 4 of 6 5 of 7 Oithona spp. 97.7% 2.34% 97.9% 2.08% 98.0% 1.98% 98.24% 1.76% 97.86% 2.14% 98.24% 1.76% 96.98% 3.02% *All species were present in all 36 samples analyzed except Oncaea dentipes (absent from 1 winter sample in 1996) O. atlantica none found in 3 winter samples (1995 and 1996) and 1 spring sample (1995) Oncaea vodjanitskii is present

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169 Discussion Comparison of BATS non calanoid sex ratios to previous studies Although very sparse, there are a few studies pertaining to the sex ratio s of non calanoid copepods. One of the most comprehensive studies, as far as the author knows, is that of Bttger Shnack et al. (1989). These investigators observed sex ratios of several species of non calanoid copepods from 2 stations in the Red Sea during fall and winter. They found the families Saphirinidae (represented by 2 genera and species) and Corycaeidae (comprised of 2 genera and 4 species) to have a consistently even average sex ratio with males > 40% of adults and averaging 50% and 55% for each f amily, respectively. These results were in agreement with, although slightly higher percentage of males than those found in the present study (31 and 32%, respectively). The family Oithonidae, however, was found to have a much higher proportion of males th an the present investigation specifically17% versus 0.21% in the case of the 200 m nets and 2.1% for the 64 200 m size fractions of the Taylor tows. However, after correcting for the presence of copepodites in the Taylor samples 64 200 m size category t he results were in agreement at 22% males. Bttger Shnack et al. (1989) calculated an overall ratio of 46% males for the larger species of Oncaeidae ( O. mediterranea O. media O. venusta and Triconia conifera ) and their results compare well to a global a verage of 32% males found in the BATS 200 m net samples, with a similar species mix. However, the observed ratio by Bttger Shnack et al. (1989) of 17% males for adult micro oncaeids ( Triconea dentipes O. zernovi and Spinoncea ivlevi ) was well below the 41% found in the Taylor 64 200 m size fraction in the present study. Only O. vodjanitskii had a male ratio similar to that of Bttger Shnack et al. (1989). A species by species comparison can also be made for 10 taxa between the pre sent study and results of Bttger Shnack et al. (1989). Adult populations of Sapphirina metallina were found to be composed of an average of 42% males in the present study compared to 55% in the Bttger Shnack et al. investigation. These authors also deter mined an adult male ratio of 48 and 60% for Corycaeus speciosus and C. limbatus respectively. These numbers are in agreement with results of the present study which

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170 found an overall of 55% males for the former and 63% for the latter species. Sex ratios de termined for Lubbokia squillimana were also reasonably close between Bttger Shnack et al. and the current examination (13.0 and 8.4%, respectively). The results of the one comparable Farranula species, F. rostrata were far different among the studies. T he prese n t investigation calculated male F. rostrata to compose an average of only 4.6% while the study of Bttger Shnack et al. estimated the ratio to be much higher (52%). However, the family with the most species in common between the studies was Oncaei dae A total of two large species O. venusta and Triconia conifera from 200 m ne t samples and three micro oncaeids T. dentipes O. zernovi Spinoncaea ivlevi from the 64 200 m Taylor samples can be directly compared. The sex ratios of O. venusta and Tr iconi a conifera were virtually identical between the present study and that of Bttger Shnack et al. Males were found to comprise 41% and 51% for O. venusta and T. conifera respectively, in the present study while they made up a similar proportion of 50% and 45% for the two species, respectively, in the investigation of Bttger Shnack et al. On the other hand the micro oncaeid copepods had vastly different sex ratios in the two studies. While the male proportion of the adult population of T. dentipes was s imilar among the two studies (39 and 48%, respectively) the same cannot be said regarding the other two species. O. zernovi as well as S. ivlevi had much lower respective proportions of males in the Bttger Shnack et al. study (6 and 2%) compared to the present ex amination ( 45 and 55%). The cause of the large discrepancy was likely the coarser mesh net used in the Bttger Shnack et al. study comp ared to the present investigation (100 vs. 20 and 35 m). Reproductive strategy influence on field observed sex ratios in copepods Aside from the way males locate females and how mating occurs, there are two main reproductive strategies employed by pela gic copepods that are inherently related to the presence or absence of seminal receptacles in the female genital segment (Kirboe, 2006). Species whose females possess seminal receptacles need to mate only one time and can store sperm to fertilize all egg batches produced for the entire lifespan of the female, whereas those without receptacles (mainly species of the super family Centropagoidea) cannot store sperm and need to mate for each clutch of eggs produced (Ohtsuka and Huys,

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171 2001; Kirboe, 2006) On e adaptive measure for members of Centropagidae to facilitate mating is swarming behavior of sexually mature adults (Kimoto et al., 1988; Ueda et al., 1983). During a zooplankton collection cruise in coastal waters off Kuwait in the Northwestern Arabian Gu lf during late March of 1999, an extremely dense surface swarm of small crustaceans was observed and sampled by the author. The swarm was later identified as being entirely composed of adult Temora turbinata a c entropagid species. In addition, the groups l acking seminal receptacles have double the fecundity of those with receptacles as well as the ability to produce resting eggs, a feat not found in species able to store sperm (Kirboe, 2006) Many copepod species that can store sperm have a highly skewed standing adult sex ratio favoring females while those that require repeated mating have near equal proportion of males and females (Svensen and Tande, 1999; Kirboe, 2007; Bttger Schnack, 1989). The rate of fertilization may constrain copepod populations as much as factors such as food availability, presence of predators and physical and chemical conditions (Kirboe, 2006). All non calanoid females have seminal receptacles, but the various groups differ markedly in their sex ratios. For example, Oithona spp. had the lowest male to female ratios of all non calanoid groups found at BATS while most Harpacticoids and Poecilostomatoid copepods had a more even sex ratio. The reason for this may be due to a precopula (a period prior to actual transfer of spermat ophores when the male clasps female) that may last days to weeks in Harpacticoids and Poecilostomatoid copepods (Lazzaretto and Battaglia, 1994). However, an exception to this general rule was Lubbokia squillamana that had a very skewed sex ratio in favor of females. Perhaps their precopula was much briefer than other members of the Poecilostomatoid copepods or that the males were more concentrated at depths greater than those sampled in the present study. Role of selective predation in shaping observed copepod sex ratios Since, as previously mentioned, it is assumed that the investment made by each parent in dioecious organisms is the same for each of the sexes produced there is no difference in the size of eggs or sperm and by extension the amount of energy invested to produce either sex it is implicit that the sex ratio would be 1:1 at the time of birth (Fisher, 1930; Charnov, 1982). However, the observed sex ratios in

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172 the field vary greatly according to family, genus as well as species and are found to even vary seasonally (Hirst and Kirboe, 2002 and references therein). Thus, the often highly skewed sex ratios favoring females (Mauchline, 1998) may be the result of differential mortality of the sexes with males suffering significantly higher rates than females of a given species. Given that the benefits of a single mating vary greatly for the two different types of copepod fertilization systems, females possessing seminal receptacles need to mate with at most two males to ensure that all eggs produ ced in her lifetime will be fertile. Thus, these females have a lower requirement for mate encounters than their counterparts lacking seminal receptacles. However, the males of the receptacle possessing species have much more to gain from a single mating t han males of those that lack seminal receptacles and are much more likely to engage in risky search behavior in order to find a mate and will therefore be more susceptible to predation and in the case of many of these species the males also do not feed li kely shortening their lif espan (Ohtsuka and Huys, 2001). Possible reasons for sex selective predation include sexual dimorphism with males generally smaller than females and with higher activity levels. Increases in swimming behavior in males render the animals more likely to encounter a predator. Circumstantial evidence for predator induced skewed sex ratios include that of the study of Hicks and Marshal (1985) while the studies of Maly (1970) and Hairston et al. (1983) demonstrated the same phenomenon t hrough field and laboratory experiments. Maly (1970) confirmed the ability of predators to influence the sex ratio of two species of freshwater calanoid copepod ( Diaptomus Shoshone and D. coloradensis ) and concluded that it was caused by a combination of s ize and behavioral differences between the genders, along with the hunting style and size preferences of the predators. A later field study by Hairston et al. (1983) of the freshwater calanoid D. sangineus and fish predators concluded that the presence of the fish significantly altered the sex ratio of the copepod, with females being preferentially eaten, especially those with attached egg sacs. Moreover, an analysis by Hicks and Marshall (1985), studying gut contents of deep sea meiobenthic harpacticoid c opepod predators, showed that at least one (Pectinacea bivalves) contained a preponderance of male harpacticoids. Thus, differential sex specific mortality could be one reason for observed biases toward female abundance. Other studies have noted the marked differences in swimming activity of the two sexes in many copepod species with males often being much more active swimmers with faster speeds and less time spent

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173 motionless (Kiorboe, 2006 and 2007). Such behavior would render them more susceptible to enco unters with predators and would, over time, change the standing sex ratio to favor females For example, Kirboe (2007) found that male Oithona davisae divide d their time equally between ambush feeding with little movement and mate searching behavior with high velocity swimming that in addition to aiding in finding a mate also increased the encounter rate s with predators. This factor is likely one of the main reasons for the adult field population being highly skewed toward females since O. davisae reared i n the lab produce near equal ratios of males to females at the time adulthood was reached (Kirboe, 2007). In addition, Kirboe concluded that the low capacity (~ 1 time per day) to mate regardless of encounter rates with females coupled with the low abund ance of males compared to females was likely the reason for the observations of Uye and Sano (1995) of a large proportion of non breeding adult females (~ 2/3 of the population). Role of sampling bias It is a well known fact that sexual dimorphism in copepods is widespread with the males usually considerably smaller than the females (DeFrenza et al., 1986; Maly and Maly, 1999; Ohtsuka and Huys, 2001). This could potentially lead to a bias towards females if the mesh size is small enough to capture the females quantitatively but large enough to allow a significant portion of the males to escape. Another sampling problem could be related to differential depth distributions for the sexes of some species. For example Hayward (1981) noted that males of the vertically migrating calanoid copepod Pleuromamma pisekii with well developed spermatophores tended to migrate to shallower nighttime depths than those without. He speculated that this might be an adaptation to increase their chances of finding a female. O ther instances of sex ratios varying with depth have been noted in the Red Sea for non calanoid copepods of the genus Oncaea Lubbockia and Corycaeus (Bttger Schnack, 1989). The authors calculated the sex ratio separately for species with bimodal depth di stribution in the upper 450 m of the water column and of 4 species with this type of vertical population structure found that O. mediterranea O. media and C. limbatus all had significantly (factors of 5.6, 5.9 and 2.3) more males in the epipelagic than i n the mesopelagic zone while L. squillimana had more males in the mesopelagic region compared to the epipelagic zone, although the difference was not as large (29% greater) as in the other three species

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174 examined. This may have some significant implication s to the sex ratios found in the present study as species with wide vertical distributions may have an overall sex ratio very different than that calculated for the upper 200 m sampled in the BATS program, especially for species of Oncae a Corycaeus and L ubbokia Another interesting puzzle, albeit not directly related to pelagic copepods, is the example of possible causes of highly female skewed sex ratios of deep sea meiobenthic harpacticoids. Earlier studies on deep sea benthic harpacticoids concluded t hat the overall sex ratio was significantly biased towards females ranging from 2.4 to 25 females for each male (Coull, 1973; Hicks and Coull, 1983; Hicks and Marshall, 1985). This contrasted with the more equitable ratios seen for meiobenthic intertidal a nd littoral harpacticoids (Hicks and Coull, 1983). However, Thistle and Eckman (1990) showed that in some of their samples local males were more numerous than females and overall had a more equitable ratio of 1male for every 2 females. The authors conclude d that previous studies may have under sampled males due to biases introduced by the sampling methods, mainly due to differential erodability of the sexes and/or vertical distribution in the sediment. Possible role of sex change on sex ratios It has long been suspected through both field and experimental investigations that environmental factors could influence sex determination in copepods (Katona, 1970; Grigg et al., 1981; Hopkins, 1982). These included abiotic factors such as temperature, pr essure, and photoperiod as well as biological aspects comprising infection by parasites, nutrition and population density. Fleminger (1985) noticed that species of the family Calanidae contained females of two distinctive morphs those with a typical female trithek A1 (1aesthetasc and 2 setae per segment) and those with a quadrithek A1 (with double the number of aesthetascs per segment) that resembles the male. He hypothesized that the quadrithek female morph was actually a genetic male that had undergone a sex change during the final molt from CV to CVI by way of hormonal secretions from the genital tract as shown to occur in malacostracan crustaceans. Fleminger (1985) studied this phenomenon in detail for the species Calanus pacificus californicus and found that most of the quadrithek females were found in late winter. The adaptive value of this gender switching by males

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175 diapauses first, thus, a male that swit ches to female would have the advantage as there is an abundance of males and a scarcity of trithek females. As time progresses and more trithek females emerge from diapauses and males become less abundant it will be more adaptive for genetic males not to switch gender but rather mate with multiple females. In an attempt to test the hypothesis of Fleminger (1985) Svensen and Tande (1999) studied the proportion of quadrithek females of Calanus finmarchicus from fall to spring over two years and found similar seasonal patterns to those determined by Fleminger. In addition, the authors noted that the proportion of the quadrithek females decreased with decreasing latitude likely due to the concomitant increases in the number of generations per year. Results of e xperiments by Svensen and Tande (1999) found the female to male sex ratio of C. finmarchicus to be a little over 6:1 when both quadrithek and trithek forms of females were included, but the ratio dropped to near 1:1 when only trithek females were deemed fe male and quadrithek forms counted as males. These authors also concluded from their experiments that the presence of adults of either sex had no influence on the proportion of quadrithek females and therefore ruled out a role for pheromone control of the a pparent sex change of C. finmarchicus Finally, a study by Irigoien et al. (2000) concluded that for all copepods the important factor in sex determination one that united all the previous disparate observations of external influences seemed to be developm ent time. The authors noted that more rapid transitions through key stages cause masculine ization while slower development leads to feminization. Summary and conclusions The sex ratio of non calanoid copepods is expected to be 1:1 at birth due to Fishe However, the marked departures from the 1:1 ratio seen in the field could be due to several factors, individually or in combination, that results in a bias towards females. These include: 1) ESD 2) change of genetically determined sex due to en vironmental cues in later development stages 3) differential sex specific mortality and 4) sampling bias introduced by using mesh sizes that allow the generally smaller males to be under sampled as well as the potential of separate depth distributions of t he sexes.

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176 Little is known for certain regarding calanoid copepod mating and causes of observed sex ratios and of what is known about these parameters very little pertains to non complicated phenomenon with wide ranging populati on and ecological consequences. Thus, this could be a very rewarding field to pursue in the future at BATS. Towards this goal, as discussed in previous chapters, it is vital that improvements be made in sampling strategy and gear used (e.g finer meshes an d more discrete depth sampling) along with more physiological experimental work done onboard the research vessel on animals collected from tows using physiological cod ends. All this must be done to produce a more complete understanding of zooplankton dyna mics and ultimately a better comprehension of elemental budgets at BATS and by extension the global ocean. After all, as mentioned by Kirboe (2008), when all is said and done, it is the interaction with the environment perceived by individual organisms an d not the abstractions of populations or trophic levels that in the end drives the large scale pelagic energy and elemental budgets.

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177 Chapter Six Overall Summary and Conclusions

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178 Results of the present study have shed light on an important component of the zooplankton at BATS. Non calanoids compose d an abundant and species rich community with a total of 57 identified species and 21 genera from 11 families and 4 orders. In addition, non calanoids were found to have a significant impact on C and N dynamics at BATS due to the fact that they were a major constituent of the zooplankton (> 13,000 copepods m 2 ) and also by associations with different floating macro particles in the epipela gic zone (0 200 m). Annual differences were found in the case of non calanoid abundance from the > 200 m size fraction. Overall, populations were generally highest in 1995 and 1999 ( Oithona Oncaeidae and Corycaeus ) while Sapphirina spp. were most numerou s in 1996 (due to one bloom cruise), otherwise they followed overall trend. Examples of other non calanoid taxa that deviated from the overall annual trend were those of Farranula spp. which had a stable population among the 5 years analyzed, and m iraciid harpacticoids that were inversely related to overall non calanoid abundance ( highest in 1997 and lowest in 1995). Seasonal signals were, in general, much stronger than annual variation. Late spring and early summer (particularly May and June) had highest abundance of overall non calanoids while lowest population densities were found in winter. Only miraciid harpacticoids were abundant in win ter and even then only early winter (January) prior to vertical mixing of the water in later in the season (February March). Other e xceptions to the general trend of peak abundance in late spring early summer were Corycaeus specious that was most abundant in fall and both Triconia minuta and Lubbokia spp with maximum densities in summer and fall Miraciid harpacticoid s were most abundant in late summer to late fall. Abundance of t otal zooplankton in the 64 200 m size fraction averaged 1.22 million individuals m 2 with the majority (> 60%) consisting of c opepod nauplii Non calanoids composed an average of 21% of total zooplankton abundance while c alanoids (mainly copepodites) made up 11% In addition, It was found that the copepod community (adults and copepodite stages) in the 64 200 m category was dominated by non calanoids (66%).

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179 Annual and seasonal patterns were noted for the microzooplankton community (64 200 m) with non calanoids most abundant in 1995 and most constituents being most numerous in late spring and lowest with some exceptions in winter. The 200 m net non calanoid copepods were estimated t o make up close to a 1/3 of overall C requirements and N excretion rates of total mesozooplankton The non calanoid taxa comprising the bulk of C and N cycling were Oithona spp ., Corycaeidae and Oncaeidae each contributing 35, 31 and 26%, respectively of the non calanoid portion When the 64 200 m size fraction was analyzed, it was found to contain an overall average of 177 mg dwt m 2 or approximately 40% of the > 200 m net biomass from the same cruises However, calculated C demand and N regeneration ra tes of the small size fraction were on a par with those of the larger size category of zooplankton and sometimes even exceeded them Comparing the C ingestion and N excretion rates to primary production rates and N requirements for production revealed the microzooplankton and mesozooplankton consumed C equivalent to 15.4% and 14.6% of daily primary production m 2 (0 150 m) and the N excretion of the microzooplankton and mesozooplankton were capable of supporting 6 and 7%, respectively, of the primary produ ction N daily requirements. The small size fraction (64 200 m) analyzed in the present study revealed a significant proportion of biomass and > 90% of non calanoid abundance is missed by 200 m mesh nets. In addition to developmental stages a large com munity of adult species was either extremely under sampled (< 5% retained by 200 m mesh) or missed entirely. Four identified and 1 unknown species of micro Oncaeidae were found. Of these four were described for the first time from the Sargasso Sea. Of al l the interesting features of non calanoid copepods none is as fascinating as the associations between some important taxa and floating organic debris represented mainly by larvacean houses, Trichode smium colonies, and to a lesser extent salps. It was calculated in the present study that oncaeid copepods were capable of removing approximately 10% of daily larvacean house production (m 2 0 200 m) and Microsetella spp could consume an overall of 7% (~ 11% for both spring and summer) of daily house produ ction. While miraciid harpacticoids grazed ~ 12% of Trichodesmium C and N standing crop on a daily basis Lastly, Sapphirina spp in particular S. angusta was found to be abundant only during salp blooms suggesting a dependence on the pelagic Thalicea.

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180 Th us, non calanoids are important components of the zooplankton, particularly the smaller size fractions, in terms of biomass and in particular abundance. In addition to their role in elemental cycling via typical zooplankton functions, a subset of taxa are particularly adapted to associate with and feed on different organic aggregates thereby playing a role in the remineralization and degradation of sinking particulate matter in the oceans Future studies at BATS should concentrate on depth resolution sampl ing, particularly at density discontinuity layers, as these are hypothesized to be regions of heightened abundance and activity of oncaeid and Microsetella spp particulate matt er degradation in the epipelagic layer Furthermore, it is necessary to employ fine mesh nets (i.e. 64 m) in order to properly sample the entire non calanoid community at BATS. Finally, in addition to better zooplankton sampling strategies, the feeding be havior and reproductive strategies of non calanoids is a promising research field with potential to shed light on the exact role of POM associated non calanoid taxa at BATS

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200 Turner JT (1986) Zooplankton feeding ecology contents of fecal pellets of the Cyclopoid copepods Oncaea venusta Corycaeus amazonicus Oithona plumifera and Oithona simplex from the northern Gulf of Mexico. Marine Ecology 7:289 302 Turner JT (2002) Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquatic Microbial Ecology 27:57 102 Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological Studies 43:255 266 Turner JT, Tester PA, Conley WJ (1984) Zooplankton feeding ecology predation by the marine cyclopoid copepod Corycaeus amazonicus f Dahl upon natural prey. Journal of Experimenta l Marine Biology and Ecology 84:191 202 Uchima M (1988) Gut content analysis of neritic copepods Acartia omorii and Oithona davisae by a new method. Marine Ecology Progress Series 48:93 97 Uchima M, Hirano R (1986) Food of Oithona davisae copepoda cyclop oida and the effect of food concentration at first feeding on the larval growth. Bulletin of Plankton Society of Japan 33:21 28 Uchima M, Hirano R (1988) Swimming behavior of the marine copepod Oithona davisae internal control and search for environment Marine Biology 99:47 56 Uchima M, Murano M (1988) Mating behavior of the marine copepod Oithona davisae Marine Biology 99:39 45 Ueda H, Kuwahara A, Tanaka M, Azeta M (1983) Underwater observations on copepod swarms in temperate and sub tropical waters Marine Ecology Progress Series 11:165 171 Urban JL, McKenzie CH, Deibel D (1992) Seasonal differences in the content of Oikopleura vanhoeffeni and Calanus finmarchicus fecal pellets illustrations of zooplankton food web shifts in coastal Newfoundland waters. Marine Ecology Progress Series 84:255 264 Uye S, Aoto I, Onbe T (2002) Seasonal population dynamics and production of Microsetella norvegica a widely distributed but little studied marine planktonic harpacticoid copepod. Journal of Plankton Resea rch 24:143 153 Uye S, Sano K (1995) Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series 118:121 128 Verity PG (1985) Ammonia excretion rates of oceanic copepods and i mplications for estimates of primary production in the Sargasso Sea Atlantic ocean. Biological Oceanography 3:249 284 Villareal TA, Carpenter EJ (1990) Diel buoyancy regulation in the marine diazotrophic cyanobacterium Trichodesmium thiebautii Limnology and Oceanography 35:1832 1837 Wada E, Hattori A (1976) Natural abundance of N 15 in particulate organic matter in North Pacific Ocean. Geochimica et Cosmochimica Acta 40:249 251 Walsby AE (1978) Properties and buoyancy providing role of gas vacuoles in T richodesmium ehrenberg British Phycological Journal 13:103 116

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201 Webber MK, Roff JC (1995a) Annual biomass and production of the oceanic copepod community off Discovery Bay, Jamaica. Marine Biology 123:481 495 Webber MK, Roff JC (1995b) Annual structure o f the copepod community and its associated pelagic environment off Discovery Bay, Jamaica. Marine Biology 123:467 479 Weikert H, John HC (1981) Experiences with a modified B multiple opening closing plankton net. Journal of Plankton Research 3: 167 176. White AE, Spitz YH, Karl DM, Letelier RM (2006) Flexible elemental stoichiometry in Trichodesmium spp and its ecological implications. Limnology and Oceanography 51:1777 1790 White JR, Zhang XS, Welling LA, Roman MR, Dam HG (1995) Latitudinal gradients in zooplankton biomass in the tropical Pacific at 140 degrees w during the jgofs eqpac study effects of El Nino. Deep Sea Research Part Ii Topical Studies in Oceanography 42:715 733 Wiggert JD, Haskell AGE, Paffenhofer GA, Hofmann EE, Klinck JM (2005) The role of feeding behavior in sustaining copepod populations in the tropical ocean. Journal of Plankton Research 27:1013 1031 Williamson CE, Butler NM (1987) Temperature, food and mat e limitation of copepod reproductive rates separating the effects of multiple hypotheses. journal of plankton research 9:821 836 Zervoudaki S, Christou ED, Nielsen TG, Siokou Frangou I, Assimakopoulou G, Giannakourou A, Maar M, Pagou K, Krasakopoulou E, Christaki U, Moraitou Apostolopoulou M (2007) The importance of small sized copepods in a frontal area of the Aegean Sea. Journal of Plankton Research 29:317 338 Zhang X, Dam HG, White JR, Roman MR (1995) Latitudinal Variations in Mesozooplankton Grazin g and Metabolism in the Central Tropical Pacific during the US JGOFS EQPAC Study. Deep Sea Research Part Ii Topical Studies in Oceanography 42:695 714 Zhang XS, Dam HG (1997) Downward export of carbon by diel migrant mesozooplankton in the central equatori al Pacific. Deep Sea Research Part Ii Topical Studies in Oceanography 44:2191 2202

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202 A ppendices

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203 A ppendix 1 : Average (standard Deviation) range and coefficient of variation (%) of volumes filtered and depths of tows for all 200 m net samples analyzed (1995 1999) Season 1995 1996 1997 1998 1999 Volume filtered (m 3 ) Winter 582 (146) 441 809 25% 621 (65) 539 696 10% 645 (216) 377 1018 33% 828 (187) 498 1000 23% 911 (627) 433 2298 69% Spring 390 (126) 241 567 32% 545 (182) 252 799 33% 597 (82) 498 734 14% 749 (339) 451 1334 45% 603 (181) 362 861 30% Summer 763 (310) 393 1126 41% 508 (233) 267 905 46% 691 (250) 441 1057 36% 525 (216) 241 791 41% 546 (123) 393 695 23% Fall 455 (45) 394 519 10% 424 (134) 283 591 32% 780 (152) 607 1022 20% 618 (212) 396 906 34% 546 (178) 310 759 33% Annual 539 (226) 241 1126 42% 518 (175) 252 905 34% 669 (187) 377 1057 28% 683 (263) 241 1334 38% 671 (386) 310 2298 58% Maximum depth sampled (m) Winter 200 (0) 200 200 0% 181 (16) 160 195 9% 202 (28) 155 250 14% 193 (27) 155 235 14% 189 (17) 160 210 9% Spring 199 (16) 165 225 8% 205 (35) 135 240 17% 218 (20) 185 240 9% 202 (35) 150 245 17% 149 (39) 93 210 26% Summer 171 (33) 118 200 19% 213 (22) 175 242 11% 170 (33) 125 215 20% 216 (33) 170 265 15% 175 (33) 135 202 19% Fall 195 (33) 160 245 17% 204 (27) 180 250 13% 205 (45) 165 292 22% 179 (35) 125 220 20% 203 (57) 114 271 28% Annual 192 (25) 118 245 13% 203 (28) 135 250 14% 200 (34) 125 292 17% 197 (34) 125 265 17% 178 (41) 93 271 23%

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204 Appendix 2 : Summary of annual average individual abundance m 2 (0 200 m) including standard deviation c oefficient of variation (%) and range for all genera (adults and copepodites) of BATS 200 m non calanoid copepod genera Genus 1995 1996 1997 1998 1999 Oithona 5,821 (4,298) 74% 1,866 15,261 3,649 (2,046) 56% 190 7,357 4,531 (2,217) 49% 1,269 10,180 4,111 (1,903) 46% 1,498 9,237 5,989 (3,678) 61% 1,170 14,925 *Oncaea 5,583 (4,315) 77% 776 15,790 4,030 (2,683) 67% 654 10,951 3,282 (1,823) 56% 235 7,493 5,211 (4,190) 80% 1,035 16,697 5,881 (4,836) 82% 330 18,588 Farranula 1,814 (1,315) 73% 164 6,026 1,775 (1,256) 71% 36 4,400 1,684 (1,259) 75% 193 4,836 2,024 (2,040) 101% 258 9,834 2,346 (1,718) 73% 112 5,709 Corycaeus 1,481 (789) 53% 55 3,796 1,146 (719) 63% 31 2,693 1,289 (948) 74% 129 3,981 1,238 (668) 54% 508 3,167 2,015 (1,253) 62% 257 4,490 Lubbokia 218 (185) 85% 0 784 202 (197) 98% 0 748 222 (153) 69% 45 714 225 (113) 50% 58 438 253 (153) 60% 0 640 Sapphirina 132 (129) 98% 0 450 186 (287) 155% 10 1,055 82 (72) 88% 0 357 104 (85) 81% 17 280 128 (181) 141% 0 699 Macrosetella 22 (29) 130% 0 127 62 (89) 144% 0 321 83 (86) 103% 0 333 33 (45) 134% 0 173 102 (98) 96% 0 296 Copilia 56 (72) 128% 0 270 77 (101) 132% 0 456 37 (30) 81% 0 89 47 (33) 72% 0 108 78 (104) 132% 0 382 Oculosetella 14 (18) 129% 0 56 11 (22) 195% 0 87 39 (44) 115% 0 197 17 (27) 158% 0 97 34 (31) 92% 0 93

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205 Appendix 2 (continued) 1995 1996 1997 1998 1999 Corissa 14 (22) 156% 0 97 12 (16) 133% 0 48 15 (18) 118% 0 65 26 (25) 96% 0 95 16 (22) 139% 0 71 Clytemnestra 25 (34) 139% 0 158 9 (13) 137% 0 45 11 (13) 125% 0 46 16 (27) 170% 0 122 22 (40) 186% 0 167 Distioculus 13 (15) 119% 0 56 5 (8) 144% 0 24 14 (23) 162% 0 81 7 (11) 160% 0 32 19 (31) 161% 0 118 Miracia 10 (28) 281% 0 127 17 (38) 230% 0 167 7 (15) 208% 0 71 6 (10) 169% 0 32 20 (28) 141% 0 115 Pontoecielia 6 (16) 268% 0 71 8 (14) 183% 0 61 4 (8) 191% 0 34 9 (12) 131% 0 36 10 (20) 212% 0 84 Microsetella 10 (30) 302% 0 141 1 (3) 490% 0 16 1 (4) 337% 0 21 18 (50) 273% 0 243 7 (12) 183% 0 34 Vettoria 3 (9) 270% 0 35 5 (8) 147% 0 24 6 (8) 127% 0 32 7 (14) 205% 0 49 6 (12) 189% 0 49 Ratania 6 (12) 211% 0 47 4 (11) 260% 0 48 3 (7) 235% 0 36 5 (13) 251% 0 54 7 (18) 261% 0 84 Pacos 1 (3) 500% 0 14 <1 (1) 490% 0 7 4 (8) 222% 0 36 2 (5) 247% 0 17 2 (11) 520% 0 58 Includes the genus Triconia Includes copepodites identified to genus level

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206 Appendix 3 : Summary of pooled seasonal average abundance m 2 (0 200 m) including standard deviation coefficient of variation (%) and range for all genera (adults and copepodites) of BATS 200 m non cal anoid copepod genera Genus Winter Spring Summer Fall Oithona 3,685 (2,424) 66% 190 13,065 6,369 (3,632) 57% 1,297 15,261 5,214 (3,071) 59% 1,607 12,518 3,745 (1,852) 49% 1,498 8,439 Oncaea* 3,714 (3,722) 100% 235 12,666 6,878 (4,136) 60% 1,627 18,588 4,950 (3,750) 76% 1,096 15,790 2,957 (1,516) 51% 812 7,008 Farranula 683 (590) 86% 36 2,117 2,705 (1,769) 65% 497 9,834 2,711 (1,339) 49% 1,015 6,026 1,553 (1,024) 66% 347 3,663 Corycaeus 644 (594) 92% 31 2,348 1,823 (968) 53% 678 4,490 1,708 (828) 48% 391 3,909 1,586 (864) 54% 619 3,981 Lubbokia 155 (118) 76% 0 471 145 (89) 62% 0 379 295 (160) 54% 63 784 343 (179) 52% 103 748 Sapphirina 94 (144) 153% 0 693 189 (247) 131% 0 1,055 94 (93) 99% 0 423 103 (72) 70% 0 357 Macrosetella 90 (92) 103% 0 333 20 (20) 150% 0 116 36 (56) 156% 0 221 112 (93) 83% 0 321 Copilia 40 (58) 144% 0 270 103 (105) 102% 0 456 39 (44) 113% 0 179 38 (35) 91% 0 133 Mormonilla 20 (37) 178% 0 172 44 (85) 192% 38 (61) 160% 0 228 33 (52) 159% 0 217

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207 Appendix 3 (continued) Genus Winter Spring Summer Fall Oculosetella 46 (44) 95% 0 197 20 (26) 133% 0 84 7 (12) 164% 0 44 20 (21) 120% 0 87 Corissa 7 (11) 155% 0 41 13 (19) 138% 0 71 21 (24) 115% 0 95 27 (24) 88% 0 97 Clytemnestra 19 (29) 159% 0 158 19 (35) 181% 0 167 12 (24) 208% 0 122 15 (19) 128% 0 74 Distioculus 17 (24) 142% 0 104 9 (16) 180% 0 81 6 (11) 187% 0 35 16 (26) 156% 0 118 Miracia 10 (22) 215% 0 115 2 (7) 328% 0 30 13 (26) 210% 0 127 26 (37) 144% 0 167 Pontoecielia 4 (9) 231% 0 34 7 (15) 231% 0 84 10 (18) 186% 0 71 9 (14) 149% 0 61 Microsetella 5 (13) 253% 0 55 4 (13) 314% 0 54 17 (51) 308% 0 243 4 (10) 238% 0 42 Vettoria 4 (10) 239% 0 49 5 (10) 211% 0 49 8 (11) 139% 0 40 6 (10) 161% 0 32 Ratania 2 (6) 264% 0 32 7 (18) 275% 0 84 4 (10) 232% 0 48 7 (12) 174% 0 48 Pacos 1 (3) 406% 0 14 1 (9) 624% 0 58 3 (6) 219% 0 22 3 (7) 280% 0 36 Includes copepodites

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208 Appendix 4 : Summary of annual and seasonal average miraciid copepod abundance m 2 (0 200 m) including standard deviation, coefficient of variation (%) and range for all 200 m net samples at BATS (1995 1999) Species 1995 1996 1997 1998 1999 Macrosetella gracilis 22 (29) 130% 0 127 62 (89) 144% 0 321 83 (86) 103% 0 333 33 (45) 134% 0 173 102 (98) 96% 0 296 Oculosetella gracilis 14 (18) 129% 0 56 11 (22) 195% 0 87 39 (44) 115% 0 197 17 (27) 158% 0 97 34 (31) 92% 0 93 Miracia efferata 10 (28) 281% 0 127 17 (38) 230% 0 167 7 (15) 208% 0 71 6 (10) 169% 0 32 20 (28) 141% 0 115 Distioculus minor 13 (15) 119% 0 56 5 (8) 144% 0 24 14 (23) 162% 0 81 7 (11) 160% 0 32 19 (31) 161% 0 118 Winter Spring Summer Fall Macrosetella gracilis 90 (92) 103% 0 333 20 (20) 150% 0 116 36 (56) 156% 0 221 112 (93) 83% 0 321 Oculosetella gracilis 46 (44) 95% 0 197 20 (26) 133% 0 84 7 (12) 164% 0 44 20 (21) 120% 0 87 Miracia efferata 10 (22) 215% 0 115 2 (7) 328% 0 30 13 (26) 210% 0 127 26 (37) 144% 0 167 Distioculus minor 17 (24) 142% 0 104 9 (16) 180% 0 81 6 (11) 187% 0 35 16 (26) 156% 0 118

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209 Appendix 5 : General tow statistics (average, standard deviation, range and % coefficient of variation) for all 20 and 35m net tows and amounts of samples analyzed (1995 1997) Volume filtered (m 3 ) Amount of tow analyzed >200 m 64 200 m 1995 (20 m net) 27 (20) 14 73 73% 2/29 (1/51) 1/16 1/8 29% 1/78 (4/883) 1/256 1/164 35% 1996 (20 m net) 21 (9) 8 40 42% 1/12 (2/65) 1/16 1/8 37% 1/45 (1/71) 1/64 1/16 64% 1997 (35 m net) 32 (16) 10 62 50% 1/14 (1/32) 1/32 1/8 44% 5/543 (3/827) 1/256 1/64 39% Winter 33 (18) 14 73 55% 5/77 (1/50) 1/32 1/8 31% 1/90 (1/224) 1/256 1/64 40% Spring 22 (13) 8 49 60% 1/14 (1/340 1/32 1/8 41% 1/78 (6/767) 1/256 1/32 61% Summer 18 (7) 10 29 36% 3/32 (1/29) 1/16 1/8 37% 1/45 (1/50) 1/128 1/16 90% Fall 32 (17) 15 62 52% 7/87 (1/33) 1/16 1/8 38% 1/60 (4/569) 1/128 1/32 42% All tows 27 (16) 8 73 58% 5/67 (2/71) 1/32 1/8 38% 9/619 (1/98) 1/256 1/16 70%

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210 Appendix 6 : Annual non calanoid average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200m size fractions) analyzed (1995 1997) Species 1995 1996 1997 (All values in thousands m 2 ) Microsetella rosea 0.87 (0.88) 101% 0 2.12 0.74 (0.94) 127% 0 3.15 0.85 (1.22) 144% 0 3.87 Microsetella norvegica 14.94 (10.84) 73% 1.71 35.94 13.23 (11.11) 84% 0 36.45 15.22 (12.84) 84% 0.76 51.21 Microsetella copepodites 8.48 (6.64) 78% 1.05 20.54 8.68 (6.31) 73% 0.28 21.11 8.39 (7.48) 89% 0 23.28 Mixed Oncaea 9.20 (10.13) 110% 1.43 37.22 3.52 (2.05) 58% 0 6.47 3.81 (2.58) 68% 0.76 11.07 1.47 (0.86) 59% 0 2.98 0.54 (0.65) 122% 0 1.91 0.87 (0.78) 90% 0 2.21 Triconia dentipes 10.31 (10.89) 106% 1.18 29.96 3.76 (2.57) 68% 0 7.42 5.00 (2.87) 57% 0.76 9.97 Spinoncaea ivlevi 33.02 (23.23) 70% 6.17 79.67 15.92 (11.88) 75% 0.75 44.39 19.81 (9.84) 50% 4.22 40.60 Oncaea atlantica 7.73 (9.26) 120% 0 32.51 3.74 (4.42) 118% 0 15.16 4.16 (3.08) 74% 0.85 12.56 Oncaea zernovi 48.67 (24.45) 50% 14.31 82.46 32.36 (18.62) 58% 5.67 72.92 22.31 (10.80) 48% 4.49 39.89 Oncaea vodjanitskii 1.51 (1.44) 96% 0 3.85 0.79 (1.20) 152% 0 3.83 1.09 (1.59) 146% 0 5.80 0.49 (0.75) 153% 0 2.18 0.25 (0.34) 136% 0 1.08 0.28 (0.40) 144% 0 0.97 Oncaeid copepodites (<300m length) 79.54 (35.16) 44% 27.32 127.06 64.98 (30.44) 47% 26.27 126.44 68.64 (27.56) 40% 15.31 123.19 Oncaeid copepodites (>300m length) 10.62 (6.07) 57% 3.34 21.67 4.78 (2.85) 60% 0.76 11.13 8.57 (6.01) 70% 2.01 23.47 Corycaeid copepodites 6.00 (5.14) 86% 0.79 15.30 5.28 (3.98) 75% 0.38 12.64 4.20 (3.81) 91% 0 14.49 Oithona spp. 90.34 (48.54) 54% 17.99 160.74 64.68 (29.46) 46% 17.58 118.37 76.10 (35.35) 46% 21.12 163.08 Includes copepodites

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211 Appendix 7 : Annual other zooplankton average individual abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200m size fractions) analyzed (1995 1997) Group or species 1995 1996 1997 (All values in thousands m 2 ) Copepod nauplii 739.5 (409.9) 55% 103.2 1,391.3 716.2 (286.9) 40% 222.8 1,217.3 761 (282.6) 37% 204.3 1,232.3 Calanoid copepodites 139.6 (75.6) 54% 39.8 246.9 102.1 (36.6) 36% 46.1 168.9 123.4 (65.8) 53% 33.8 289.4 Calanoid spp. 16.08 (11.36) 71% 2.78 36.53 10.67 (6.44) 60% 1.70 20.97 18.97 (7.46) 39% 4.19 27.24 Larvaceans 59.57 (58.97) 99% 2.10 197.1 46.0 (33.35) 72% 17.93 127.77 37.49 (24.55) 65% 9.50 83.30 Radiolaria 13.38 (7.50) 56% 2.76 26.95 10.61 (6.02) 57% 1.76 20.33 11.97 (6.60) 55% 2.33 28.99 Foraminifera 5.59 (8.29) 148% 0 26.02 4.20 (6.68) 159% 0 22.34 3.06 (4.38) 143% 0 17.14 Tintinids 16.97 (16.44) 97% 0 55.19 9.14 (7.66) 84% 0.28 26.70 7.33 (8.13) 111% 0 27.82 Gastropod 5.25 (3.54) 68% 0.53 11.98 8.35 (6.23) 75% 1.71 21.17 7.59 (7.26) 96% 0 23.19 Pelycepod larvae None found 0.05 (0.14) 256% 0 0.45 0.07 (0.19) 274% 0 0.67 Chaetognath larvae 0.57 (0.60) 105% 0 1.57 0.99 (1.05) 106% 0 3.59 0.40 (0.61) 152% 0 1.56 Mesusa larvae 1.19 (2.53) 213% 0 7.62 0.80 (0.91) 114% 0 3.00 0.62 (0.69) 112% 0 2.35 Polychate larvae 1.29 (1.51) 117% 0 3.85 1.96 (2.46) 126% 0.19 9.20 0.88 (0.78) 89% 0 2.90 Doliolid larvae 0.20 (0.34) 180% 0 1.04 None Found 0.20 (0.45) 221% 0 1.34 Ostracod 3.71 (2.92) 79% 0.53 7.83 2.83 (2.73) 97% 0 8.12 2.04 (1.96) 96% 0 6.76 Creisis None found 1.27 (3.69) 291% 0 12.94 None found Noctiluca None found None found 0.04 (0.15) 374% 0 0.57 Salp None found 0.30 (0.43) 145% 0 1.18 None found Siphonophore 0.06 (0.20) 316% 0 0.64 0.06 (0.22) 346% 0 0.75 None found Barnacle nauplii None found 0.10 (0.35) 346% 0 1.21 None found

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212 Appen dix 8 : Seasonal non calanoid average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200m size fractions) analyzed (1995 1997) Species Winter Spring Summer Fall (All values in thousands m 2 ) Microsetella rosea 0.44 (0.77) 173% 0 2.12 0.50 (0.64) 130% 0 1.79 1.42 (1.30) 91% 0.48 3.87 1.47 (1.22) 83% 0 3.15 Microsetella norvegica 6.89 (6.14) 89% 0 19.83 18.99 (10.93) 58% 3.42 36.45 22.95 (14.92) 65% 10.58 51.21 14.87 (9.67) 65% 5.28 28.15 Microsetella copepodites 3.36 (2.82) 84% 0 8.35 10.00 (5.76) 58% 2.14 20.54 15.19 (6.24) 41% 9.26 23.28 10.23 (7.30) 71% 2.90 21.11 Oncaea scottodicarloi 0.83 (1.07) 130% 0 3.65 1.04 (0.93) 89% 0 2.97 1.27 (0.84) 66% 0.57 2.86 0.73 (0.59) 81% 0.24 1.91 Mixed Oncaea 3.59 (2.87) 80% 0 10.44 8.83 (10.30) 117% 2.73 37.22 3.24 (1.64) 51% 1.43 5.80 4.73 (1.86) 39% 1.58 7.65 Triconia 0.60 (0.72) 120% 0 1.93 0.99 (1.10) 111% 0 2.98 1.20 (0.77) 64% 0 1.93 1.20 (0.55) 45% 0.48 1.91 Triconia dentipes 4.67 (6.31) 135% 0 23.31 5.99 (6.49) 108% 1.79 23.10 6.27 (2.11) 34% 2.84 8.71 8.56 (9.64) 113% 2.38 29.57 Spinoncaea ivlevi 20.35 (13.87) 68% 0.75 40.60 21.48 (16.62) 77% 8.07 65.46 18.25 (7.53) 41% 6.61 27.82 29.97 (25.00) 83% 4.22 79.67 Oncaea atlantica 2.92 (2.89) 99% 0 7.87 3.74 (2.94) 79% 0 10.27 5.79 (3.89) 67% 1.70 12.56 10.05 (10.84) 108% 2.42 32.51 Oncaea vodjanitskii 0.81 (1.07) 132% 0 2.91 1.24 (1.40) 113% 0 3.85 1.25 (2.25) 179% 0 5.80 1.33 (1.41) 106% 0 3.83 0.17 (0.40) 197% 0 0.97 0.38 (0.70) 206% 0 2.18 0.30 (0.42) 137% 0 0.97 0.61 (0.45) 73% 0 1.28 Oncaeid copepodites (<300m) 68.13 (31.84) 47% 27.32 123.19 86.29 (27.25) 32% 41.16 127.06 54.26 (24.77) 46% 26.27 82.33 66.00 (32.21) 49% 15.31 108.67 Oncaeid copepodites ( >300m) 8.47 (6.92) 82% 2.01 23.47 8.36 (3.89) 47% 4.45 16.69 5.43 (2.91) 54% 0.77 8.70 8.16 (6.97) 85% 2.39 21.67 Corycaeid copepodites 2.26 (1.80) 80% 0 5.80 7.01 (4.17) 59% 1.95 12.84 6.77 (5.11) 76% 1.91 14.49 6.01 (4.68) 78% 0.79 15.30 Oithona spp. 79.96 (46.47) 58% 17.99 163.08 91.70 (28.20) 31% 56.91 127.38 56.90 (26.88) 47% 17.58 84.03 63.85 (36.33) 57% 21.12 130.66 Includes copepodites

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213 Appendix 9 : Seasonal other zooplankton average abundance (0 150 m) data including standard deviation, coefficient of variation (%) and range for all Taylor tows (64 200m size fractions) analyzed (1995 1997) Species Winter Spring Summer Fall (All values in thousands m 2 ) Copepod nauplii 649.2 (282.9) 44% 103.2 1,087.6 891.7 (303.6) 34% 471.6 1,391.3 609.1 (296.1) 49% 222.8 1,035.8 804.6 (358.5) 45% 204.3 1,217.3 Calanoid copepodites 148.0 (73.9) 50% 39.8 289.4 106.7 (47.2) 46% 39.4 188.4 94.3 (30.7) 33% 46.1 136.2 120.2 (61.3) 51% 33.8 211.6 Calanoid spp. 16.84 (9.99) 59% 4.19 36.53 15.34 (6.62) 43% 6.42 26.57 14.11 (8.52) 60% 1.70 22.78 13.97 (11.43) 82% 2.78 32.51 Larvaceans 50.51 (49.97) 99% 2.10 197.08 37.23 (31.40) 84% 8.36 101.25 53.67 (40.39) 75% 15.75 127.77 45.95 (31.20) 68% 9.50 100.07 Radiolaria 9.11 (5.11) 56% 2.33 18.77 12.86 (7.81) 61% 1.76 26.95 14.29 (7.32) 51% 10.01 28.99 13.69 (5.97) 44% 6.60 20.33 Foraminifera 5.16 (5.28) 102% 0.66 17.14 3.63 (6.86) 189% 0 22.34 0.91 (1.30) 144% 0 3.35 5.76 (9.40) 163% 0 26.02 Tintinids 6.05 (9.28) 153% 0 29.23 15.65 (14.42) 92% 5.29 55.19 12.46 (11.74) 94% 2.46 27.82 10.32 (7.93) 77% 1.06 21.67 Gastropod larvae 3.56 (2.34) 66% 0 7.45 11.06 (7.21) 65% 1.71 22.27 9.93 (7.57) 76% 1.43 23.19 6.08 (3.80) 63% 1.85 13.53 Pelycepod larvae None found 0.05 (0.14) 316% 0 0.45 0.14 (0.27) 188% 0 0.67 0.04 (0.12) 265% 0 0.31 Chaetognath larvae 0.42 (0.56) 131% 0 1.57 1.19 (1.14) 95% 0 3.59 0.38 (0.61) 158% 0 1.34 0.49 (0.43) 87% 0 1.21 Mesusa larvae 0.67 (1.13) 167% 0 3.65 1.68 (2.29) 137% 0 7.62 0.22 (0.45) 206% 0 1.14 0.47 (0.39) 83% 0 0.97 Echinoderm larvae 0.63 (1.14) 180% 0 3.41 0.22 (0.56) 255% 0 1.76 0.16 (0.25) 155% 0 0.48 0.48 (0.78) 163% 0 2.15 Polychate larvae 0.75 (0.97) 129% 0 2.90 1.38 (1.20) 87% 0 3.85 0.78 (0.82) 106% 0 1.91 2.92 (2.92) 100% 0.79 9.2 Doliolid larvae 0.08 (0.29) 361% 0 1.04 0.15 (0.36) 239% 0 1.11 0.22 (0.55) 245% 0 1.34 0.14 (0.25) 181% 0 0.64 Ostracod 1.91 (2.45) 128% 0 7.83 3.35 (2.42) 72% 0 8.07 2.63 (2.23) 85% 0.67 6.76 3.63 (3.10) 85% 0.53 8.12 Creisis None found 1.37 (4.07) 298% 0 12.94 None found 0.22 (0.27) 125% 0 0.54 Noctiluca None found None found 0.10 (0.23) 245% 0 0.57 None found Salp 0.11 (0.30) 274% 0 1.05 0.16 (0.38) 238% 0 1.18 None found 0.08 (0.21) 265% 0 0.54 Siphonophore 0.06 (0.21) 361% 0 0.75 None found None found 0.09 (0.24) 265% 0 0.64

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214 Appendix 10 : Overall, annual and seasonal respiratory carbon estimates of all copepod adult and larval stages for 64 200 m size fraction (0 150 m) of all Taylor tows at BATS Taxon Overall n = 36 1995 n = 10 1996 n = 12 1997 n = 14 Winter n = 13 Spring n = 10 Summer n = 6 Fall n = 7 Copepod nauplii 2.97 *(2.56 3.39) 2.96 (1.93 3.99) 2.90 (2.20 3.60) 3.05 (2.47 3.62) 2.52 (1.92 3.11) 3.47 (2.73 4.22) 2.55 (1.63 3.48) 3.47 (2.29 4.65) Calanoid copepodites 7.60 (6.36 8.84) 8.72 (5.81 11.6) 6.47 (5.13 7.81) 7.77 (5.63 9.92) 8.99 (6.53 11.5) 6.22 (4.42 8.03) 6.27 (4.69 7.86) 8.12 (5.0 11.2) Calanoid spp. 2.12 (1.72 2.52) 2.19 (1.22 3.17) 1.47 (0.97 1.97) 2.62 (2.08 3.17) 2.23 (1.52 2.95) 2.05 (1.49 2.62) 2.04 (1.05 3.04) 2.07 (0.80 3.33) Microsetella spp. 2.51 (1.89 3.13) 2.57 (1.46 3.67) 2.37 (1.36 3.39) 2.58 (1.43 3.74) 1.10 (0.65 1.55) 2.94 (1.95 3.94) 4.26 (2.35 6.18) 3.01 (1.68 4.34) Oncaea spp. a 1.87 (1.33 2.40) 3.16 (1.61 4.71) 1.26 (0.85 1.68) 1.46 (1.02 1.90) 1.30 (0.68 1.92) 2.37 (0.88 3.87) 1.78 (1.33 2.24) 2.27 (1.00 3.54) Oncaea spp. b 3.02 (2.46 3.58) 4.44 (3.09 5.79) 2.69 (1.90 3.49) 2.28 (1.83 2.73) 3.09 (2.08 4.10) 3.30 (2.49 4.11) 2.22 (1.45 2.99) 3.17 (1.34 5.00) Oncaea copepodites c 2.51 (2.13 2.89) 2.96 (2.11 3.81) 2.13 (1.57 2.69) 2.51 (1.92 3.09) 2.41 (1.70 3.13) 2.89 (2.31 3.47) 1.96 (1.32 2.60) 2.60 (1.53 3.66) Oithona spp. d 2.55 (2.15 2.96) 3.00 (2.02 3.98) 2.19 (1.63 2.75) 2.55 (1.96 3.13) 2.59 (1.79 3.39) 3.00 (2.43 3.57) 2.00 (1.30 2.71) 2.32 (1.31 3.33) Corycaeid copepodites 0.25 (0.18 0.32) 0.30 (0.13 0.46) 0.27 (0.15 0.38) 0.21 (0.11 0.31) 0.11 (0.06 0.15) 0.34 (0.21 0.47) 0.35 (0.14 0.56) 0.32 (0.13 51) Others e 0.20 (0.14 0.26) 0.25 (0.12 0.38) 0.20 (0.08 0.33) 0.17 (0.10 0.24) 0.10 (0.03 0.17) 0.25 (0.16 0.34) 0.20 (0.08 0.33) 0.32 (0.10 0.53) All copepods all stages 25.6 (22.1 29.1) 30.5 (21.9 39.2) 22.0 (17.5 26.5) 25.2 (20.2 30.2) 24.4 (18.3 30.6) 26.8 (21.7 32.0) 23.7 (16.5 30.9) 27.7 (16.4 38.9) 95% confidence intervals of the mean a) Medium Oncaea spp. ( O. scottodicarloi b) Micro Oncaea ( O. zernovi O. vojanitskii O. atlantica Triconea minuta T. dentipes and Spinoncaea ivlevi ) c) Includes both small and large categories (i.e. < 300 and > 300 m total length) d) Includes copepodites e) Unidentified non calanoid copepodites Mormonilla minor Pontoecielia ayssicol Corisa parva Corycaeus brehmi, Farranula rostrata and early copepodites of Sapphirina Lubbokia and Miraciid harpacticoids

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215 Appendix 11 : Overall, annual and seasonal inorganic nitrogen excretion estimates of all copepod adult and larval stages for 64 200 m size fraction (0 150 m) of all Taylor tows at BATS Taxon Overall n = 36 1995 n = 10 1996 n = 12 1997 n = 14 Winter n = 13 Spring n = 10 Summer n = 6 Fall n = 7 Copepod nauplii 0.56 *(0.48 0.64) 0.56 (0.36 0.75) 0.55 (0.42 0.68) 0.57 (0.47 0.68) 0.47 (0.36 0.59) 0.65 (0.51 0.79) 0.48 (0.31 0.66) 0.66 (0.43 0.88) Calanoid copepodites 1.30 (1.09 1.52) 1.49 (0.99 1.99) 1.11 (0.88 1.34) 1.33 (0.97 1.70) 1.54 (1.12 1.96) 1.07 (0.76 1.38) 1.08 (0.81 1.35) 1.40 (0.86 1.93) Calanoid spp. 0.35 (0.29 0.42) 0.37 (0.20 0.53) 0.25 (0.16 0.33) 0.44 (0.35 0.53) 0.37 (0.25 0.49) 0.34 (0.25 0.44) 0.34 (0.18 0.51) 0.35 (0.13 0.56) Microsetella spp. 0.42 (0.32 0.53) 0.43 (0.25 0.62) 0.40 (0.23 0.57) 0.43 (0.24 0.63) 0.18 (0.11 0.26) 0.49 (0.33 0.66) 0.72 (0.40 1.04) 0.51 (0.28 0.73) Oncaea spp. a 0.31 (0.22 0.40) 0.53 (0.27 0.79) 0.21 (0.14 0.28) 0.24 (0.17 0.32) 0.22 (0.11 0.32) 0.40 (0.15 0.64) 0.30 (0.22 0.37) 0.38 (0.17 0.59) Oncaea spp. b 0.52 (0.42 0.62) 0.77 (0.53 1.00) 0.46 (0.33 0.60) 0.39 (0.32 0.47) 0.53 (0.36 0.71) 0.57 (0.43 0.71) 0.38 (0.25 0.52) 0.55 (0.23 0.87) Oncaea copepodites c 0.44 (0.37 0.50) 0.52 (0.37 0.66) 0.37 (0.28 0.47) 0.44 (0.34 0.54) 0.42 (0.30 0.55) 0.50 (0.40 0.61) 0.34 (0.23 0.46) 0.45 (0.27 0.64) Oithona spp. d 0.45 (0.38 0.52) 0.52 (0.35 0.70) 0.38 (0.29 0.48) 0.45 (0.34 0.55) 0.45 (0.31 0.59) 0.52 (0.42 0.62) 0.35 (0.23 0.48) 0.41 (0.23 0.59) Corycaeid copepodites 0.04 (0.03 0.06) 0.05 (0.02 0.08) 0.05 (0.03 0.07) 0.04 (0.02 0.05) 0.02 (0.01 0.03) 0.06 (0.04 0.08) 0.06 (0.03 0.10) 0.06 (0.02 0.09) Others e 0.03 (0.02 0.05) 0.04 (0.02 0.07) 0.03 (0.01 0.06) 0.03 (0.02 0.04) 0.02 (0.01 0.03) 0.04 (0.03 0.06) 0.03 (0.01 0.06) 0.05 (0.02 0.09) All copepods all stages 4.41 (3.81 5.02) 5.25 (3.76 6.74) 3.79 (3.01 4.57) 4.34 (3.49 5.20) 4.21 (3.16 5.27) 4.62 (3.74 5.51) 4.08 (2.82 5.32) 4.77 (2.84 6.70) 95% confidence intervals of the mean a) Medium Oncaea spp. ( O. scottodicarloi b) Micro Oncaea ( O. zernovi O. vojanitskii O. atlantica Triconea minuta T. dentipes and Spinoncaea ivlevi ) c) Includes both small and large categories (i.e. < 300 and > 300 m total length) d) Includes copepodites e) Unidentified non calanoid copepodites, Mormonilla minor Pontoecielia ayssicol Corisa parva Corycaeus brehmi, Farranula rostrata and early copepodites of Sapphirina Lubbokia and Miraciid harpacticoids

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About the Author Hussain Al Mutairi received his Bachelor of Science in Zoology from Kuwait University in 199 2 He worked as a laboratory instructor at the Kuwait University Department of Zoology from 1992 1993. From 1993 2002 Hussain worked for the Kuwait Institute for Sci entific Research (KISR) in the Oceanography group of the Departme nt of Mariculture and Fisheries. During his time with KISR Hussain received a full scholarship from KISR to complete his MS in Oceanography and was awarded a MS in Biological Oceanography from the University of Hawaii at Manoa in 1999. His advisors include d Michael R. Landry and David M. Karl. In 2002 Hussain received a scholarship from the Kuwait Public Authority for Applied Education and Training (PAAET) to obtain a Ph.D. in Marine Science at the University of South Florida, College of Marine Science. Mr Al Mutairi has authored and coauthored several refereed journal articles and has presented at several international conferences.


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Title from PDF of title page.
Document formatted into pages; contains 215 pages.
Includes vita.
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Dissertation (Ph.D.)--University of South Florida, 2009.
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Includes bibliographical references.
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Text (Electronic dissertation) in PDF format.
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ABSTRACT: Zooplankton were sampled on a monthly basis at the Bermuda Atlantic Time-series Study (BATS) site from January 1995 to December 1999. Samples were collected using a 1-m, 200 m mesh net. The net sampled the water column in an oblique manner from the surface to a mean depth of 200 m. One day and one night tow from each cruise was examined microscopically to determine the community structure of the non-calanoid copepods. In addition, a three year set of nighttime samples were examined taken by 0.5-m, 20 and 35 m mesh nets (1995-1996 and 1997, respectively) towed obliquely to 150 m. The dominant orders in terms of overall abundance were the Cyclopoida and Poecilostomatoida. The cyclopoid genus, Oithona, was most abundant followed by the Poecilostomatoid family, Oncaeidae, and the genera Farranula and Corycaeus. Harpacticoids, although common, were about an order of magnitude less abundant and were dominated by Macrosetella gracilis.Representatives of the Mormonilloida and Siphonostomatoida also were frequently encountered, although in much lower numbers. Overall, pronounced seasonal signals were noted; highest abundances occurred during spring and lowest during winter. However, abundance of some groups peaked either in the fall or winter, with lowest abundance in spring or summer. Miraciid copepods are estimated to consume an overall average of 359 g C m d and regenerate 55 g N m d derived from Trichodesmium at BATS. Highest grazing and regeneration rates were found in late summer through fall and early winter and lowest in spring and early summer. The ecological consequences of miraciid copepod feeding on Trichodesmium are discussed. The 20-35 m net samples revealed an astonishing abundance of non-copepod species, some totally missed and others woefully under-sampled by the 200 m net.At least four species of oncaeid copepods and the harpacticoid copepod Microsetella norvegica were found in abundances that were more than an order of magnitude higher than the corresponding numbers of non-calanoid copepods sampled by the 200 m net. The role of all non-calanoid copepods, from both net systems, in C and N dynamics at BATS is analyzed and discussed along with the sex-ratios of most identified species.
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Mode of access: World Wide Web.
System requirements: World Wide Web browser and PDF reader.
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Advisor: Joseph Torres, Ph.D.
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C: N-cycling
Trichodesmium
Macrosetella
Oncaea
Microzooplankton
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Dissertations, Academic
z USF
x Marine Science
Doctoral.
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t USF Electronic Theses and Dissertations.
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u http://digital.lib.usf.edu/?e14.3215