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Distribution, Metabolism and Trophic Ecology of the Antarctic Cydippid C tenophore Callianira antarctica West of the Antarctic Peninsula by Kerri M. Scolardi A thesis submitted in partial fulfillment of the requirements for the degree of Maste r of Science College of Marine Science University of South Florida Major Professor: Kendra L. Daly, Ph.D. Joseph J. Torres, Ph.D. George Matsumoto, Ph.D. Date of Approval: March 25 2004 Keywords: Southern Ocean, gelatinous zooplankton, respirat ion, digestion, ROV Copyright 2004, Kerri M. Scolardi
Acknowledgements This research was supported by NSF grants OPP 9910610 and OPP 0196489 (K Daly), OPP 9910100 (J Torres), and an AAUS scholarship (K Scolardi). The results reported in this thesi s were made possible through collaboration with a number of investigative groups involved with the SO GLOBEC program. Respira tion data were contributed by Joseph J. Torres and J oe Donnelly (USF), excretion data were provided by K ent Fanning and S teve Bell (USF), S e J ong Chu and Rodger Harvey (UMCES) provided lipid analysis, and Scott Gallager (WHOI) and the WHOI Sea Rover team made under ice video images available for ctenophore distribution analysis. I would also like to acknowledge J ohn Klinck and E ilee n Hoffman (OD U ), and C arin Ashjian, Scott Gallager, and Peter Wiebe (WHOI), who graciously shared their results and sampling instruments Also, Evgeny Pakhomov provided unpublished data on Callianira antarctica ingestion rates during autumn 2001. I am gr ateful to E mily Yam, J ason Zimmerman, J oe Donnelly, Christian McDonald, Joel Bellucci, Melanie Parker, Stian Alesandrini, Tom Bailey, Gealin Rosenwacks, P hillip Alatolo, D icky Allyson, E rik Chapman, and G areth Lawson for their assistance with experimental work, data collection and data analyses I extend my warmest appreciation to my many other GLOBEC shipmates who provided moral and technical support, encouragement and friendship. I would also like to thank the AAUS scholarship committee for supporting g raduate students and their research. Lastly, and most importantly, I would like to thank my Masters thesis committee Dr. Kendra Daly, Dr. Joseph Torres and Dr. George Matsumoto, whose constant support, guidance and patience is deeply appreciated.
i Tabl e of Contents List of Tables iii List of Figures iv Abstract vi Chapter One 1 Introduction Chapter Two 5 Materials and Methods Sampling platforms and study area 5 Sampling 8 Distribution and abundance 10 Chemical composition 11 Met abolic rates 11 Estimation of digestion time 12 Lipid composition 1 4 Gut contents 14 Statistical analysis 14 Chapter Three 16 Length Frequency and Vertical Distribution Results Length frequency 16 Horizontal distribution 17 Vertica l distribution and abundance 18 Discussion Length frequency 22 Distribution and abundance 25 Chapter Four 29 Chemical Composition, Metabolism, and Feeding Ecology Results Chemical composition 29 Metabolic rates 31 Feeding behav ior 33 Digestion time 34
ii Lipid storage 40 Lipid biomarker analysis 41 Gut contents 47 Discussion Chemical composition 50 Metabolic rates 52 Maintenance carbon rations and body turnover 55 Feeding ecology: experimental 56 Feedi ng ecology : in situ 62 Chapter Four 65 Summary References 67 Bibliography 76
iii List of Tables Table 1 Collection information and analysis performed on C allianira antarctica for each field season 9 Table 2 Cal lianira antarctica Total length, dry weight (DW), and water content as percent of the DW for autumn and winter 2002 30 Table 3 Oxygen consumption and ammonium excretion rates for Callianira antarctica and 7 other species of ctenophore 32 Table 4 Ave rage dry weight (DW), body carbon (C) and body nitrogen (N) values for each stage of prey used in digestion time experiments 35 Table 5 Callianira antarctica. Digestion stage categories defined from winter 2002 digestion time experiments 37 Table 6 C allianira antarctica. Fatty acid and alcohol composition (% of total f atty acid and alcohol) of ctenophores s ampled during autumn and winter, 2002 43 Table 7 Fatty acid ( FA ) and alcohol (ALC) compositions (% of total fatty acid and alcohol ) of potent ial prey items for Callianira antarctica 44 Tab le 8. S terol composition (% total concentration) of Callianira antarctica and their potential prey 46
iv List of Figures Figure 1 Location of study area near Marguerite Bay (MB), west of the An tarctic Peninsula 6 Figure 2. Station locations for the autumn 2002 process cruise (A) and approximate station locations for winter 2001 & 2002 survey cruises (B). 7 Figure 3. Callianira antarctica. Aboral l ength s of ctenophores measured for eac h station in (A) autumn and (B) winter. 16 Figure 4. Callianira antarctica Length frequency for autumn (A) and winter (B) 2002. 17 Figure 5. Callianira antartica Presence/absence of ctenophores over the study area during (A) winter 2001, (B) autum n 2002 and (C) winter 2002 19 Figure 6. Callianira antarctica. Diel vertical distribution during winter 2002 measured for 13 stations total (5 day and 6 night). 21 Figure 7. Callianira antarctica. Depth integrated abundance ( m 2 ) over the study area during winter 2002. 24 Figure 8. Callianira antarctica The seasonal relationship between total length and (A) dry weight and (B) carbon concentration for autumn (filled symbols) and winter (open symbols) 2002. 29 Figure 9. Callianira antarcti ca The seasonal relationship between dry weight and (A) total carbon and (B) total nitrogen for autumn (filled symbols) and winter (open symbols) 2002. 30 Figure 10. Callianira antarctica The relationship between oxygen consumption (circles), ammoni um excretion (squares) and dry weight. 32 Figure 11. Callianira antarctica. Images of Euphausia superba in the ctenophore stomodeum during digestion Stage (from top left to bottom right ) I II III/IV and V of digestion. 37
v Figure 12. Callianira an tarctica Digestion stage intervals (h) for each experiment in relation to ctenophore length. 38 Figure 13. Callianira antarctica. C tenophore length versus (A) digestion time and (B) weight specific digestion rate. 38 Figure 14 Callianira antarcti ca The relationship between total digestion time and ingested prey (A) dry weight, (B) total carbon, and (C) total nitrogen content. 39 Figure 15. Callianira antarctica Number of prey ingested versus total digestion time. 40 Figure 16. Calliani ra antarctica Percent increase in lipid volume measured in guts of C. antarctica after digestion of prey. 41 Figure 17. Total lipid content and lipid class compositions (PL=Polar lipids, CS=Cholesterol, FFA=Free fatty acids, TG =Triacylglycerols, WE =Wax esters, FALC= Free fatty alcohols) of ctenophores and their potential prey sampled during autumn ( A ) and winter ( B ) 42 Figure 18. Callianira antarctica Gut contents of ctenophores collected during three field seasons; from left to right: winter 2 001 (n = 20), autumn 2002 (n = 43), and winter 2002 (n = 82). 49 Figure 19. Callianira antarctica Prey type making up the recognizable prey portion of gut contents from ctenophores collected during three seasons: winter 2001 (n = 23), autumn 2002 (n = 18), winter 2002 (n = 13). 49 Figure 20. Relationship between digestion time and incubation temperature for ctenophores. 57
vi Distribution, Metabolism and Trophic Ecology of the Antarctic Cydippid C tenophore Callianira antarctica West of the Antarctic Peninsula Kerri M. Scolardi ABSTRACT The distribution, abundance, chemical composition, metabolism, and feeding ecology of the tentaculate ctenophore, Callianira antarctica (Chun 1 89 7) were investigated during austral winter 2001and au tumn & winter 200 2 in the vicinity of Marguerite Bay west of the Antarctic Peninsula. C allianira antarctica had a widespread distr ibution during autumn and winter and variable abundance (0.02 to 2.6 ind. m 2 ) during winter 2001 associated with specific circulation features. Size frequency distributions for autumn and winter suggest that more than half of the C. antarctica population may have experienced degrowth during winter due to low food availability C allianira antarctica is a fairly robust cten ophore with geo me tric mea n (geomean) carbon (C) and nitrogen (N) values of 8.41 and 1.83% dry weight (DW), respectively. Winter oxygen consumption and ammonium excretion rates ranged from 0.059 to 0.410 l O 2 [mg DW] 1 h 1 and 0.60 to 31.1 g at N [g DW] 1 h 1 respectively, at 0 o C. Daily minimum maintenance rations based on respiration experiments were 2.7% to 3.6% of the total body carbon (TBC) for small ctenophores, and 1.4% to 1.9% TBC for larger ctenophores Calanoid copepods and larv al and juvenile Antarctic krill were offered to ctenophores in incubation experiments Digestion times were variable, lasting 8 to 20 h and were independent of ctenophore size and dependent on number and type of prey. Gut content analysis from
vii one autum n and two winter seasons indicated C. antarctica preyed on both copepods and krill in situ with a n increased dependence on larval krill during winter. Lipid biomarker analysis on C. antarctica and their potential prey confirmed these result s. D ivers obs erved aggregations of C. antarctica passively drifting with tentacles extended near dense concentrations of larval Euphausia superba during winter. These observations along with gut content and lipid biomarker analysis suggest that larval krill is an impo rtant prey item for C. antarctica during winter.
1 CHAPTER ONE INTRODUCTION The first scientific accounts of ctenophores in Antarctic waters were recorded in the late 1800s and early 1900s ( Chun 1897, Moser 1909: as referenced in OSullivan 1986). More than a century later, our knowledge of Antarctic ctenophores and their role in the Southern Ocean ecosystem has only marginally improved. The lack of information on ctenophores is in part due to the fact that their delicate, gelatinous bodies are ea sily destroyed by most collection and preservation techniques (Harbison et al. 1978, Purcell 1988). The episodic nature of ctenophore populations, owing to their rapid growth rates and high fecundity (Reeve & Walter 1976, 1978, Harbison et al.1978, Swanbe rg & Bmstedt 1991a), has also made it difficult to quantify the abundance of these organisms. More recent studies indicate that ctenophore densities in Antarctic seas display substantial seasonal and interannual variability (Lancraft et al. 1989, 1991), a nd at times may dominate total zooplankton biomass regionally ( Williams et al. 1986, Pakhomov 1989, Pags et al. 1996 1997 ). For example, Voronina et al. (1994) reported that ctenophore biomass in the 0 200 m layer of oceanic stations in the Atlantic sec tor of the Antarctic increased from 1.7 to more than 40% of the total zooplankton biomass between summer and autumn. In addition, Kaufmann et al. (2003) reported that Callianira spp. was one of three dominant macrozooplankton species making up 30 35% o f the zooplankton biomass on a dry weight basis, during early winter and spring 2000 in a small embayment of Deception Island just west of the Antarctic Peninsula.
2 Despite these recent developments, investigations concerning the role of ctenophores in t he Antarctic ecosystem are lagging behind those done for most other geographic regions. The Black Sea has received considerable attention over the last decade due to the adverse ecological changes that have taken place as a result of a number of anthropog enic factors combined with invasions of non endemic species of ctenophore into the region (see review in Kideys et al. 2000). Research related to the Black Sea has been published on everything from estimates of ctenophore abundance, distribution, growth a nd feeding rates, reproduction, and chemical composition to association s with physical feat u res and prey abundances. Similar research has been done with ctenophores from the tropics (Kremer 198 2 Kremer et al. 1986a &b Reeve et al. 1989), temperate region s ( Hirota 1974, Ikeda 1974, Kremer 1977, Larson 1987a, Larson 1987b, Larson 1987c, Youngbluth et al. 1988, Bailey et al. 1994 Purcell et al. 1994 ) and the arctic (Percy & Fife 1981, Hoeger 1983, Percy 1988, Percy 1989, Swanberg & Bmstedt 1991a, Swanberg & Bmstedt 1991b). Because ctenophores are voracious predators and exhibit rapid population growth, their trophic impact on an ecosystem is of particular interest. Ctenophores in many regions of the ocean have been shown to have a marked predatory impac t on copepods, euphausiids, and fish eggs and larvae (Reeve &Walter 1978, Greene et al.1986, Suthers & Frank 1990, Mills 1995, Purcell 1997, Shiganovoa & Bulgakova 2002, Shiganovoa et al. 2003). For instance Larson (1987a) estimated that the tentaculate ctenophore Pleurobrachia bachei and two species of medusae from the Saanich Inlet, BC, consumed 10 to 40% of Euphausia pacifica eggs and nauplii stock a day. The cydippid ctenophore Mertensia ovum which is the dominant biomass macrozooplankter in regio ns
3 of the Canadian Arctic (Percy 1988, Swanberg & Bmstedt 1991a,1991b, Siferd & Conover 1992), is considered to be an important predator on crustacean zooplankton. Elsewhere, field and laboratory studies on the widely distributed cydippid ctenophore Pleu robrachi a pileus indicate that this species has the potential to seriously impact zooplankton populations where it exists (Reeve et al. 1978, Frank 1986, Chandy & Greene 1995, Bmstedt 1998). In situ observations of Antarctic ctenophores under sea ice s uggest that ctenophores may play a larger trophic role in the Antarctic ecosystem than previously believed. Euphausia superba is a keystone species in the Southern Ocean, thus a number of top predators such as seals, penguins and whales depend entirely or to a large extent on it as a food source (Fraser & Trivelpiece 1996, Costa & Crocker 1996). Numerous studies have been conducted on the impact of these top predators on adult krill, however little is known about predation on larval krill. Substantial numbers of larval and juvenile krill are associated with the under sea ice habitat during autumn and winter (Daly 199 0 ). Daly and Macaulay (1991) suggested that ctenophores may be important predators on overwintering larval Antarctic krill, E superba ba sed on diver observations of ctenophores feeding on larvae under sea ice during autumn and winter in the Scotia Weddell seas. Hamner et al. (1989) and Hamner & Hamner (2000) also reported diver observations of the cydippid ctenophore, Callianira antarctic a under ice floes preying on larval krill during early autumn west of the Antarctic Peninsula. The presence of these predators in close proximity to the under ice habitat and associated aggregations of larval krill could have a significant influence on t he annual recruitment of larval krill
4 Before the trophic impact of ctenophores on zooplankton populations in the Antarctic region can be reliably estimated a better understanding of their ecology must first be achieved. The opportunity to do the latter arose during a series of Southern Ocean Global Ecosystem Dynamics Program (SO GLOBEC) research cruises in austral autumn and winter of 2001 and 2002 to the Marguerite Bay region, w est of the Antarctic Peninsula where divers once again observed large numbe rs of the ctenophore C antarctica in the water column just below ice associated aggregations of larval krill. SO GLOBEC is a collaborative research effort designed to examine the physical, chemical and biological processes that contribute to the abund ance and success of the Antarctic krill. Marguerite Bay west of the Antarctic Peninsula (WAP) is a physically dynamic environment marked by unusually high Antarctic krill production and a n important habitat for krill predators, making this an ideal stud y site for the program For my Masters thesis, I investigat ed the distribution, abundance and trophic ecology of C antarctica in vicinity of Marguerite Bay during autumn and winter. T he seasonal size frequency and broad scale distribution of these cten ophores, as well as their vertical distribution and abundance in the water column during the winter 2002 season are described. The elemental composition of ctenophores over autumn and winter are reported and applied to metabolic rates measured for one wi nter season to estimate daily maintenance rations. Lastly, t he trophic relationship between C. antarctia and potential prey is investigated using winter digestion rate s seasonal measurements of ctenophore l ipid composition and identification of biomarker s in their potential prey and in situ diet analys e s in autumn and winter
5 CHAPTER TWO MATERIALS AND METHODS Sampling platforms and study a rea. Data were collected during three cruises to the Antarctic during austral autumn and winter as part of the U.S. Southern Ocean GLOBEC Program in the vicinity of Marguerite Bay, west of the Antarctic Peninsula (Fig. 1). Two research vessels operated jointly in the study area during austral autumn and winter expeditions in 2001 and 2002. The RV Lawrence M. Gou ld concentrated on a small number of selected sites for extended durations (Fig. 2A) while the RVIB Nathaniel B. Palmer conducted a broad scale grid survey of the study area (Fig 2 B ) Data for this project were obtained aboard the RV Lawrence M. Gould d uring a n autumn process cruise (7 April to 20 May 2002) and aboard the RVIB Nathaniel B. Palmer during two winter survey cruises (24 July to 31 August 2001 and 31 July to18 September 2002). The study area, roughly located between 65 o to 72 o S and 72 o to 64 o W, is bound to the north by Adelaide Island and to the south by Alexander Island with Marguerite Bay in the middle (Fig. 1) During winter, nearly the entire survey area was covered with pack ice that was particularly thick in the southeastern porti ons of the survey grid Sea ice cover was considerably less in the autumn generally limited to waters deep within Marguerite Bay and along the coastline Although most of the sampling was concentrated over shelf waters generally <500m in depth certain bathymetric features, such as the cross shelf Marguerite trench located in the center of the study area, and deep
6 water canyons in the northeast portions of the grid, as well as a number of stations at the shelf break (>3000m) provided sampling over deeper water. Figure 1. Location of study area near Marguerite Bay (MB), west of the Antarctic Peninsula. From: Howd et al. (2001). A simplified description of the water mass structure over the study area during autumn and winter is as follows: During the autumn 2002 cruise, Antarctic Surface Water (AASW) was present in the upper 100 to 120 m with temperatures ranging from 0 to 0.5 o C and in some areas a subsurface minimum water mass ( 0.5 to 1. 8 o C ) known as Winter Water (WW) resided below it Below the permanent pycnocline, typically from 1 2 0 to 150 m, a cooled form of Upper Circumpolar Deep Water (UCDW) occurred over the shelf (150 to 400m) This modified CDW results from i ntrusions of UCDW onto the shel f which subsequently mixes with the cooler surface waters These water masses are characterized by warmer temperature s ( 1.0 2.0 C), higher salinity (34.70 to 34.72), and
7 are thought to provide an u pward diffusive flux of heat salt and nutrients ( US SO GLOBEC 2002 ) The on shelf intrusions of CDW occurred just west of Adelaide Island and in the central region of the study area, overlying the Marguerite Trough. Extreme surface cooling and ice freezing in winter 2001 & 2002 led to the erosion of the AASW and formation of the colder ( 1 .8 C ) and saltier (>34 ppt) WW at the surface. A general clockwise circulation pattern persisted over the study area, starting with a strong northeastward flow associated with the Antarctic Circumpolar Current (ACC) along the shelf break a strong southwestward flow along the coast of Adelaide Island and into Marguerite Bay and a flow similar in magnitude out the southern portion of Ma rguerite Bay around Alexander Island ( Klinck et al. in press ). Lastly, a mesoscale gyre characterized by a weak clockwise flow was located over the shelf in the northern portion of the study area during each cruise ( Klinck et al. in press) Figure 2. Station locations for the autumn 2002 pro cess cruise (A) and approximate station locations for winter 2001 & 2002 survey cruises (B). The dark grey bathymetry lines running from northeast to southwest represent the shelf break.
8 Sampling. On board the Gould and Palmer t he following equipment an d methods were used to sample ctenophores and their prey: a 1.5 m 2 Tucker trawl having a 6.4 mm mesh graded down to a 707 m mesh with a protected cod end, typically towed obliquely within the upper 200 m of the water column and 1 m 2 and 10 m 2 MOCNESS (Mu ltiple Opening/Closing Net and Environmental Sensing System) equipped with 335 m and 3 mm mesh nets, respectively, towed obliquely from the surface to near bottom, sampling the entire water column with the first net on the down cast and on the up cast sa mpling discrete depth intervals with the remaining nets (Ashjian et al. in press ) Nets were towed at a speed of 1.5 to 3 kts behind the ship, ice permitting. During winter 2002, ctenophores and their prey were also collected using a 1 m diameter Reev e N et (333 m mesh net) with a 20 L protected cod end kept afloat with s yntactic foam, and a 1 m diameter r ing n et (333 m mesh). The Reeve Net and r ing n et were deployed in tandem to about 10 and 15 m depth, respectively, while the propellers were run at 15 25% to keep water circulating into the nets, but with little forward ship movement or ice sweep down into nets. This method retrieved animals in exceptionally good condition. Ctenophores collected by net tows were immediately separated from the catch once on board, and gently placed in a bucket of 0.1 or 0.2 m filtered seawater at or near sea surface temperature ( 1.8 to 0 o C). Ctenophores were also hand collected by SCUBA divers under sea ice during winter 2001 and 2002. SCUBA dives were operate d out of zodiacs and utilized a standard blue water diving rig, with a few modifications to accommodate the shallow nature of under ice specimen collection. Divers collected ctenophores from the upper 10 m of the water column by gently rotating a pre fill ed 20oz plastic Quarpac jar over the ctenophore and
9 slowly screw ing on the lid, as described by Heine (1986). Once at the surface, the jars were placed in buckets of seawater to prevent the containers of water from freezing and injuring the ctenophores. SCUBA dives were generally conducted during mid afternoon hours Ctenophores for live experiments were collected primarily with relatively short, near surface net tows or by divers. A list of analys e s performed and tow/dive information is given in Table 1. Table 1. Collection information and analysis performed on C allianira antarctica for each field season. CS=Crystal Sound, RI=Renault Island, LF=Laubeuf Fjord, Sb=Shelf break, TT= Tucker Trawl, MOC =MOCNESS Analysis Season Collection Method Stations Gut Content Winter 2001 TT, SCUBA 15, 19, 22, 71 Analysis Fall 2002 TT George VI LF Winter 2002 TT, 1 m and 10 m MOC 4, To 4, 5, 11, 13, 14, 16, Drift Net, SCUBA 17 23, 26, 40 to 28, 44, 45, 62 to 48, 65, 66/67, 72, 75, To 81, RI2 Chemical Fall 2002 TT Sb George VI LF Composition Winter 2002 TT, 1 m MOC, 4, To 4, 5, 9, 13, 16, 17, Drift Net, SCUBA 23, 26, 28, 34, 49, RI 2 Lipids Fall 2002 TT LF Winter 2002 TT, 1 m MOC, 4, 16, 26, 40 to 28, 49, 65 Drift Net Re spiration Winter 2002 TT, 1 m MOC, 4, To 4, 14, 16, 17, 23, 26, Drift Net, SCUBA 28, 34, RI 2 Digestion Winter 2002 TT, 1 m MOC; 4, 17, 62 to 48, 65, 66/67 Time Drift Net, SCUBA Vertical Winter 2002 1 m and 10 m MOC CS, 9, 11, 13, 16, 22, 26, Di stribution 42, 44, 65, 72, 75
10 Distribution and abundance. To determine t he distribution of C antarctica throughout the study area, presence/absence data was recorded from net collections conducted during the three field seasons. In addition, i n situ distribution observations of ctenophores and larval krill under ice were mad e from WHOI SeaRover ROV deployments on both winter cruises. ROV deployments most often occurred during late evening/ early morning hours, however a few deployments were done during afternoon or early evening hours. Vertical distribution and depth integra ted abundance of ctenophores during winter 2002 was determined using discrete tow data from both the 1 m 2 and 10 m 2 MOCNESS nets. Both net systems were equipped with flow meters so that total volume water filtered could be recorded and ctenophore abundanc e calculated for each depth interval The poor condition of ctenophores in preserved samples from the first two cruises precluded obtaining accurate counts of ctenophores caught in the nets, therefore on the last cruise a concerted effort was made to reco rd ctenophore counts on board. Under ice vertical distribution and densities of C. antarctica were obtained during SCUBA dives at two stations during the 2002 winter cruise. This was accomplished with a primary diver swimming 10 meter horizontal transects at 0, 2, 4, 6, 8 and 10 meters below the ice. Depth was measured using a depth gauge attached to a square meter sampler. A safety diver attached a visible chain 10 meters in length to the undersurface of the ice for the primary diver with the square met er sampler to swim beneath. A second diver swam beside the primary diver recording the number of ctenophores that passed through the square meter on a dive slate. One horizontal swim was done for each depth interval.
11 Chemical composition. Only ctenophor es in good condition were analyzed for chemical analysis. Total length (distance from the mouth to the tip of the aboral keels) oral aboral length (distance from the mouth to the anal pore), and width were measured to the nearest mm while the ctenophore was suspended in a large petri dish filled with filtered sea water. After draining the seawater from the petri dish, the ctenophore was gently blotted with a kimwipe to remove excess water and frozen at 80 o C. After returning to the laboratory, individua l ctenophores were placed in pre weighed aluminum boats and weighed to the nearest 0.1 mg. Specimens were then dried at 60 o C until a constant dry weight (DW) was achieved. Dried ctenophores were homogenized, sub sampled, and then analyzed for Carbon (C) and Nitrogen (N) content by the University of California Santa Barbara (UCSB), Marine Science Institute Analytical Laboratory. Metabolic rates. Active and undamaged ctenophores collected during winter 2002 were used for respiration and excretion experimen ts. Animals were primarily collected from the upper 10 m of the water column either by divers or drift nets. In situ temperatures in the northern half of the study area, where collection for respiration experiments was concentrated, ranged vertically fro m 1.8 o C just below the ice to ca 2 o C in deeper water (typically >200 m). Oxygen (O 2 ) consumption rates were measured on individual ctenophores using sealed vessel respirometry (Ikeda et al. 2000). O 2 concentrations were monitored continuously for about 24 h using a 30 channel oxygen electrode system as the animals reduced the oxygen in sealed, water jacketed chambers to intermediate (~ 30 mm Hg) partial pressures. Electrodes were calibrated using air and nitrogen saturated seawater at experimental tempe rature. Ctenophores were kept in the dark and water temperature was
12 maintained at 0.5 o C ( 0.1 o C) using a refrigerated water bath. Once respiration experiments were completed, all but two of the ctenophores, which were subsequently used for digestion tim e experiments, were frozen at 80 o C. O 2 consumption rates were calculated over thirty minute intervals following the initial excitatory period, which was usually one to two hours, and above the critical oxygen partial pressure (30mm Hg) for the animal. T he values for each interval were then summed and averaged over the entire time period to give a mean respiration rate for each individual. Water from the respiration chambers was subsampled and analyzed immediately for ammonium excretion, or frozen at 20 C and analyzed within a week of collection. Ammonium samples were analyzed following methods described in Gordon et al. (1993). Individual ctenophores were placed in preweighed aluminum boats, weighed to the nearest 0.1 mg, and then dried at 60 o C. The dried remains of the individuals were homogenized and analyzed for C/N and ash content as described above. Estimation of digestion time. Active and undamaged ctenophores were placed in individual polypropylene jars containing 0.1 m filtered seawater and incubated in the dark in a large flow through aquarium at in situ sea surface temperature ( 0.59 to 1.82 C). Small ctenophores were kept in 500 ml containers and medium to large ctenophores in 960 ml containers. After a 24 hour starvation period, individual ctenophores were placed into a 500 ml polypropylene jar containing prey in 0.1 m m filtered seawater and returned to the flow through aquarium. Juvenile and larval euphausiids ( E superba or T hysanoessa macrura ) and small cala noid copepods were used as prey. Experimental containers were checked hourly until the ctenophore ingested prey (T o ). After ingestion, the ctenophore was placed in a 500 or 960 ml container (depending on its size) of filtered
13 seawater, and once again inc ubated in the flow through aquarium. The digestion process was observed hourly for the first two to three hours of the experiment. Progress of digestion determined the frequency of subsequent observations in order to minimize disturbance. During each in spection, the ctenophore was gently scooped out of the jar using a medium sized petri dish and viewed under a dissecting microscope under dim light. The condition of the prey was noted The ctenophore was placed into a fresh container of filtered seawate r after each inspection. The old water from the container was filtered through a 20 m mesh sieve and any remaining material was back washed into a small petri dish and examined under a dissecting microscope for egested matter. The experiment continued u ntil there were no recognizable prey remains in the stomodeum and infundibulum, and no further material was egested. Six out of seven of the animals were used in multiple experiments, with each one preceded by a 24 h starvation period. Animals that refus ed to feed and had not ingested anything within 48 hours of the termination of the previous experiment were measured and frozen at 80 o C. Digestion time was defined as the time elapsed between ingestion of prey and clearing of the gastrovascular cavity, e stimated to the nearest hour. In order to express digestion time in terms of ingested prey C, N, or DW, prey species of the same stage and/or size as those used in the digestion experiments were sorted, measured for length, and frozen at 80 o C In the la boratory, individual euphausiids and grouped copepods (3 small or 2 large), were placed onto preweighed, combusted filters, and wet weights (WW) determined to the nearest 0.001 mg. Specimens were then placed in combusted glass vials and dried at 60 o C to a constant weight. Two of the Thysanoessa macrura samples were ground and sub sampled, while the remainder of the euphausiid samples
14 were cut in half and analyzed separately. For these samples, the %C and %N values for each individual were estimated as an average of the two halved values. The copepods and their filters were analyzed whole. Prey samples were analyzed for C/N at UCSB. Lipid composition. Ctenophores collected in nets were measured for total length to the nearest mm and their guts removed to reduce bias. Potential p rey specimens were also collected measured and/or staged. Ctenophore and prey samples were immediately frozen and stored at 8 0 C until analysis could be performed at shore based facilities. Before lipid analysis, wet weights o f ctenophore and prey samples were measured by thawing and briefly rinsing with Nano pure water. A subset of ctenophore and prey samples were then dried at 60 C for 48 hrs for measurements of water content which were then used to convert wet weight of th e animals to dry weight values. Lipid s were extract ed and analy zed by the Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science A detailed description of lipid extraction methods and analysis is given in Ju et al. (su bmitted) Gut contents. Ctenophores in good condition were analyzed for gut contents within two hours after collection. Individual ctenophores were measured for total length to the nearest mm, and gut contents examined either by dissection of the ga strovascular cavity or by suction removal of the gut contents by a pipette inserted into the gastrovascular cavity. Prey items were identified to the lowest possible taxonomic category In order to reduce biased results due to possible net feeding, prey that were newly ingested and had not reached the proximate half of the stomach were eliminated from the final count. Statistical analysis. Much of the data reported here were not normally distributed, therefore the median and range were used to describe the central trend of those data. For
15 percentage and rate measurements, the geometric mean (Laws & Archie 1981, Zar 1990), labeled as geomean throughout the text and tables, was reported if the value was different from the calculated arithmetic mean. Corr elation and regression analyses were calculated at the 5% significance level.
16 CHAPTER THREE LENGTH FREQUENCY AND VERTICAL DISTRIBUTION RESULTS Length frequency. The o ral aboral length s of 45 and 8 6 ctenophores from autumn and winter 20 02 respectively, were measured to determine size distribution. There was a similar wide range in length s of C antarctica collected in both autumn (11 mm to 90 mm) and winter (7 to 92 mm) and no apparent relationship between length and geographic locati on (i.e. north central or southern portions; Fig. 3 ). 0 20 40 60 80 100 7 5 5 5 5 5 2 4 4 4 4 4 4 4 Avian Island CS Laubeuf Shelf break George VI Sta.6 0 20 40 60 80 100 0 10 20 30 40 50 60 70 80 90 North Central South Size (mm) Size (mm) 0 20 40 60 80 100 7 5 5 5 5 5 2 4 4 4 4 4 4 4 Avian Island CS Laubeuf Shelf break George VI Sta.6 0 20 40 60 80 100 0 10 20 30 40 50 60 70 80 90 North Central South Size (mm) Size (mm) Figure 3. Callianira antarctica. Aboral lengths of ctenophores measured for each station in (A) autumn and (B) winter. CS=Crystal Sound. B A
17 Although the size ranges were similar between seasons, the dominant length classes were distinctively different (Fig. 4). A majority of the animals collected during autumn were medium sized adults with 48. 9% of the individuals in the 40 50 mm length range and < 2% smaller than 20 mm The mean length for au tumn ctenophores was 45.4 mm. A greater number of small animals were collected during winter ( > 20% smaller than 20 mm in length ) ; however the frequency distrib u tion for this season indicates that there were two length classes with modes centralized aro und 20 mm and 60 mm (Fig. 4) Figure 4. Callianira antarctica Length frequency for (A) autumn and (B) winter 2002. Horizontal distribution. The presence/absence of ctenophores over the study area during the three sampling periods is shown in Fig 5 For b oth winter seasons, there was a broad distribution of C. antarctica extending over large portions of the study area. Ctenophores were found in the north, south and central regions of the study area, on the shelf and at the shelf break, and nea r the coasts of Adelaide and Alexander Islands The lack of observations inside Marguerite Bay in Fig. 5 C is due to thick pack ice prohibiting the ship from reaching stations in this area, and therefore does not indicate an absence of A B
18 ctenophores in this region. This wide ranging distribution of ctenophores suggested ctenophore occurrence was not governed by physical features of the study area, such as bathymetry, hydrography, or ice edge. During winter 2002, 31 of the 94 net tows/ROV deployments did not catch/observe a single ctenophore, however none of the 41 stations sampled were absent of ctenophores In other words, ctenophores were present at all of the stations sampled, but were not sampled by all of the net tows/ROV deployment s done at that stati on ; indicating small scale spatial and temporal variability (Fig. 5C) The same assessment cannot be made for winter 2001 because only those stations where ctenophores were collected/observed were recorded. The autumn cruise occupied a much smaller numbe r of stations for longer periods of time (Fig 2 B ), thus, the area covered was greatly reduced compared to the winter surveys. However, the decreased extent of the pack ice allowed for sampling deeper within Marguerite Bay as well as in the smaller fjord s and sounds located behind and in the vicinity of Adelaide Island. Similar to winter 2002, ctenophores were found at all stations sampled in autumn : on and off the shelf, in Marguerite Bay, and along the coasts of Adelaide and Alexander Islands (Fig. 2 B ) Once again, ctenophore s had a heterogeneous temporal distribution as 21 of the 5 4 net tows recorded did not collect ctenophores, although ctenophores were present at every station sampled. Vertical distribution and abundance. Discrete depth tows dur ing winter 2002 indicated a broad range in vertical distribution (0 5 00 m) for C antarctica though most of the ctenophores occurr ed within and around the pycnocline (120 150 m ; Fi g. 6 ) N early the entire water column was sampled with all but two of the tows over relatively shal low shelf waters (ca 500 800 m) The two net tows conducted in waters depths
19 greater than 1000 m did not catch any ctenophores deeper than the deepest depth interval sampled on the shelf. The re were a similar number of net tows conducted during the day (n=5) and night (n=6) allowing for discernment of the diurnal distribution of C. antarctica During the day, ctenophores were concentrated within the u pper 200 m of the water column, with peak abundance at 150 200 m (3.8 ind m 3 x10 3 ). Ctenophore distribution reached deeper depths at night, though most of the ctenophores were still concentrated in the upper 250 m of the water column, with two depth maxima at 0 50 m (1 7 ind m 3 x10 3 ) and 1 00 200 m ( 2. 7 ind m 3 x10 3 ) Fig ure 5. Callianira antartica. Presence/absence of ctenophores over the study area during (A) winter 2001, (B) autumn 2002 and (C) winter 2002. The filled circles indicate locations where ctenophores were observed/collected and hollow triangles indicate absen ce. A C B
20 Integrated abundances were generally low, < 3.0 m 2 but variable between stations (Fig. 7). The lowest abundances (< 0.10 ind m 2 ) were found in deeper water at the shelf break, and the highest (> 1.0 ind m 2 ) we re located at two stations further on shelf, at the north and south ends of the study area. Circulation patterns over the shelf, as illustrated by the d ynamic topography calculated at the surface relative to 400 m, reveals a large closed gyre located over northern section of the study area (Fig. 7). The station with gre atest abundance (2.6 ind m 2 ) of ctenophores, Station 16, was located within this large clockwise flowing gyre located off of Adelaide Island. The other station of notable abundance was located offshore from Alexander Islan d in the southern area of the study region High numbers of c tenophores may have been entrained in the southwestward flow that was evident over the shelf during autumn and winter of 2001 & 2002 (Klinck et al. in press) and advected to this region from th e north ; hence leading to the elevated abundance relative to those stations located closer to the shelf break. Under ice vertical distribution and abundance was only sampled at t wo dive locations in winter 2002 I had anticipated sampling at a number of dive stations in both autumn and winter but due to the high number of tasks needing to be carried out in a limited amount of dive time, combined with the number of complicating issues involved with d iving in the Antarctic there were limited opportunitie s to complete the under ice sampling. Also, ctenophores were absent from the upper 10 meters of the water column at dive stations during autumn. O f the two stations completed, a ctenophore was counted in one 10 m transect at 5 10 m depth. General observ ations were noted for each dive during both winter and autumn seasons. Based on these observations higher abundance of ctenophores (ca 0.5 2 m 3 ) and aggregations of larval krill under the ice were present
21 over most of the study area during winter 2001 There was a complete absence of ctenophores and a paucity of larval krill under the sea ice during autumn 2002 During winter 2002, relatively high numbers of ctenophores and krill were once again seen, although much reduced in comparison with the first winter. In addition, juvenile krill seemed to be as abundant under the sea ice as larval krill during winter 2002, which was not the case in winter 2001. These observations are similar to ones made from ROV deployments during both winter seasons INDIVIDUALS 1000m 3 0 50 100 200 300 500 DAY NIGHT 1.0 2.0 3.0 4.0 0 DEPTH (m) INDIVIDUALS 1000m 3 0 50 100 200 300 500 DAY NIGHT 1.0 2.0 3.0 4.0 0 DEPTH (m) Fig ure 6. Callianira antarctica. Diel vertical distribution during winter 2002 measured for 13 stations total (5 day and 6 night). The pycnocline is indicated by the shaded area located between 150 200m.
22 DISCUSSION Length frequency. The wide range in cteno phore lengths found over autumn and winter for C. antarctica is not uncommon for polar species of ctenophore, and may represent the presence of multi year classes. Oral aboral lengths of less than 10 to greater than 50 mm have been reported for M. ovum fr om the A rctic (Percy 1989, Swanberg & Bmstedt 1991 b Siferd & Conover 1992 ) for summer, autumn and winter. Their persistent presence and length distribution over many seasons suggests that M ovum is a l ong lived species possibly two or more years ( Perc y 1989). The same could be true for C. antarct ic a however sampling during spring and summer months would be needed to confirm this. Ctenophore length s did not appear to be related spatially with the different region s or physical features (i.e. ice edge) of the study area In the Arctic Swanberg and Bmstedt (1991 b ) found larger M. ovum at the ice edge and smaller animals in open water The less turbulent waters within the pack ice would provide a more favorable environment for larger gelatinous organ isms, therefore we would expect to see a difference in the sizes of organisms inhabiting ice covered versus open water. In this study, the abundance of ctenophores off shore was reduced and fewer animals were measured; consequently t he small sample size s for each station did not permit estimation of mean lengths for these different regions, which could have indicated such a relationship. Ctenophore lengths c hange d seasonally from a unimodal distribution in autumn to a bimodal distribution in winter. The mean ctenophore length during autumn, 45.4 mm, fell directly between the small er (10 40 mm ) and large r (50 70 mm ) size cohorts for winter This type of bimodal size distribution, usually suggestive of a recent reproductive
23 event, is uncommon for winter p opulations of ctenophores although Pleurobrachei pileus from the B lack S ea was shown to have two reproductive events a year, including one in winter (Mutlu & Bingel 1999) Spawning in ctenophores can be prolonged, as in the case of M. ovum, where ctenoph ore eggs in Resolute Passage can be found over most of the year; however, large numbers of these eggs are only found between spring and summer (Siferd & Conover 1992). Egg production in ctenophores is highly dependant on food supply (Reev e et. al 1989) an d temperature ( Kremer 1994, Sullivan et al. 2001, Weisse et al. 2002 ) both of which are reduced in the upper water column in the A ntarctic during autumn and winter ( Siegel 1988, Lancraft et al. 1991 Ashjiaan et al. in press ) Therefore it is unlikely, a lthough not impossible, that the two size cohorts are due to a reproductive even t occurring in late autumn /early winter. The bimodal length frequency for winter may have also been the result of a portion of the ctenophore population experiencing degrowth During times of low food availability ctenophores are known to metabolize their own body tissue, causing them to shrink in size (Reeve & Walter 1978). Ashjian et al. (in press) report ed a significant reduction in zooplankton biomass in the Marguerite Bay region from autumn to winter 2001 ; thus it is possible that C. antarctica were suffering from decreased prey availability and utilizing internal reserves. However, a portion of the population may have e xperience d growth, as indicated by the larger siz e cohort. The circumstances causing the success of some of ctenophores and the starvation of others is not clear, however the patchy food environment may be one such variable One last and very possible explanation for the bimodal length frequency is tha t the population sampled during autumn may not have been the same one sampled during winter Although this is alwa ys a possibility when sampling ma r in e population s the
24 different sampling strategies used between autumn and winter further complicate s matte rs Autumn collections were intensified at stations closer to the coastline of Adelaide and Alexander Islands, with not as much coverage provided mid shelf and in southern portions of the study area, whereas winter sampling close to shore and in the fjord regions was hindered by heavy pack ice. Despite the fact ctenophore l ength s did not appear to be related to region in either season, it is possible that different length frequency distribution s for autumn and winter 2002 resulted from sampling different populations. Figure 7. Callianira antarctica. Depth integrated abundance (m 2 ) over the study area during winter 2002. The circles specify stations where abundance was measured with net tows and are colored according to their relative abundance. T he station of highest abundance designated by the red star, is associated with the large clockwise gyre, as illustrated by the dynamic topography calculated at the surface relative to 400 m. The dominant circulation features shown with the dynamic topo graphy in this figure for autumn 2002 were similar to those occurring in winter (Klink pers comm. ). 1.0 1.5 2.0 3.0 15.0 30.0 # / 100 m 2
25 Distribution and abundance. C allianira antarctica occurred mostly with in the upper 200 meters of the water column during bo th day and night hours, though diurnal difference s in depth maxima w ere observed. During the day ctenophore abundance gradually increased down to about 150 to 200 m, where the maximum abundance occurred. In contrast, ctenophore abundance at night decreased from a sub maximum concentr ation at 0 50 m down to about 100 to 200 m, where the largest abundances were found. Lancraft et al. (submitted) observed a similar depth distribution pattern during autumn for C. antarctica in Croker Passage : a shallow and deep depth maxima during the ni ght and during the day a single depth maxima near that of the deeper night time depth maxima Both day and night depth maxima for C. antarctica in this study were located within and just below the pycnocline, where greater concentrations of prey may acc umulate. Vertical distributions described for Callianira spp. in the A ntarctic have shown increased ctenophore concentrations at depths where zooplankton prey are found in abundance I n Port Foster, Deception Island, Callianira spp. remained in the 100 1 50 m depth range coincident with Euphausia crystallorphias and E. superba during early winter and with M etridia gerlach e i during early summer (Kaufmann et al 2003). In Croker Passage, C. antarctica, Thermisto gaudichaudi and E. superba were the only zo oplankton species, in addition to salps, to occur in surface waters at night during autumn. C allianira antarctica in the Marguerite B ay region during winter may concentrate at shallow er depths during the night to increase their pre dation effort on larval krill associated with the under ice surface, as was observed during nighttime ROV deployments However, this behavior was also observed during SCUBA di ves conducted during daytime hours L arval krill
26 and copepods in the Antarctic are not known to under g o diel vertical migration (DVM), thus it is unlikely that ctenophores were following a DVM pattern of their prey. Hence the increased concentration of ctenophores in the surface waters may have been due to other unknown factors. T he volume of water sam pled for all six night tows was twice the volume sampled during daytime tows. Therefore diurnal differences in c tenophore distribution may have been an artifact of sampling. The depth integrated abundances of C. antarctica were variable but low, with th e largest abundance (2.6 ind m 2 ) two orders of magnitude greater than the smallest (0.02 ind. m 2 ). The horizontal distribution of these abundances over the study area indicated that higher numbers of ctenophores were associated with the large clockwise gyre occupying the northern portion of the shelf, and lower numbers occurr ing over the shelf break, where the strong northeast flow associated with the ACC may disperse ctenophores in this region L ocal hydrology and topography interact to produce retenti ve features, such as gyres, that support entrapment of gelatinous zooplankton into large aggregations (Graham et al. 2001). For example, in the summer of 1979, Pags et al. (1994) found high abundances of gelatinous zooplankton in the eastern part of the Weddell Gyre. The spatio temporal horizontal distribution of P. pileus over a number of seasons was found to be related to the general circulation of the Black Sea, where high concentrations of ctenophores were found at the northern peripheries of anti cy clonic eddies (Mutlu & Bingel 1999). H igher densities of C. antarctica were also found in the southern shelf region of the shelf, where th e southwestward flow from Marguerite Bay may advect large numbers of C. antarctica to this region Ashjian et al. (i n press) reported elevated abundances of zooplankton over the southern shelf region located in the
27 southwestward current during autumn and winter of 2001. Large a ggregation s of C. antarctica coinciding with elevated abundances of krill and copepods occurr ing in the southern shelf region or within the northern shelf meso scale gyre may have a distinct predatory impact on these populations Th e mean abundance for C. antarctica (0.45 ind m 2 ) during winter was much lower than values reported for other cteno phores from temperate and tropical regions during different seasons For instance, a bundance of P. pileus in the Black Sea during winter was as high as 696 ind m 2 (Mutlu & Bingel 1999) In the Norwegian Sea P. pileus sampled during summer had a mean ab undance of 12.4 ind m 2 and a maximum abundance of 111 ind m 2 ( Bmstedt 1998) P leurobrachia pileus off Southwestern Nova Scotia was found in similar abundance, although there were extreme inter annual variations ( Frank 1986 ) C allianira antarcticas m ean abundance was also an order of magnitude lower than that of the Arctic ctenophore M. ovum Percy (1989) found that t he A rctic ctenophore M ovum from Frobisher B ay ha d a stable population structure, with similar mean abundances in summer and winter, 4 .2 and 3.4 ind m 2 respectively M ertensia ovum in R esolute P assage was also shown to have a low winter and summer abundance, although m aximum abundance during spring was as high as 911 ind m 2 ( Siferd & Conover 1992) However, th e mean abundance for th is species in the Barents Sea during spring was low, 0.95 ind m 2 (Swanberg & Bamstedt 1991b). Th ese observations demonstrate the large variability in M. ovum abundance over the Arctic. The same may be true for Callianira sp as Lancraft et al. (1991, s ubmitted) reported a much lower mean winter (0.016 ind m 2 ) and autumn abundance (0.034 ind m 2 ) for the Scotia Sea and Crocker Passage than was seen in the WAP region during this study.
28 In this study, C antarctica was the dominant ctenophore found in a utumn and winter for both years. Their predator s Beroe sp. were uncommon during these sampling periods The lack of abundance data from other season s prohibits making an accurate evaluation of the population structure of C. antarctica in the Marguerite B ay region Nevertheless, C. antarcticas widespread distribution during both autumn and winter combined with fact that this species along with Beroe sp. is the predominant ctenophore mentioned in reports concerning zooplankton ecology in this and nea rby regions indicate that this species like M. ovum in the Arctic, is a persistent member of the zooplankton community in waters w est of the Antarctic Peninsula
29 CHAPTER FOUR CHEMICAL COMPOSITION, METABOLISM AND FEEDING ECOLOGY RESULTS Chemical composition. A total of 32 C antarctica 8 from autumn and 24 from winter 2002, were measured for total length, WW, DW, and C/N content. The seasonal relationship between length and dry weight for C. antarctica is shown in Fig. 8 A Autumn ct enophores ranged in length from 3 5 .0 to 83.6 mm, with a median length of 46.5 mm (Table 2 ). Dry weights ranged from 149.9 to 757.6 mg and average d 3.9% ( 0.8 SD) WW. Water accounted for 96 to 98% WW during autumn. Winter ctenophores ranged from 8.5 to 98.0 mm in length and had a median length of 25.5 mm (Table 2 ). Dry weights ranged from 2.8 mg to 1.4 g, and averaged 4.4% ( 0.5 SD) WW. Water comprised 94 to 97% WW for winter ctenophores. The average ash content of ctenophores (n = 9) during winter was 78.9% ( 0.03 SD) DW. 0 200 400 600 800 1000 1200 1400 1600 1800 0 20 40 60 80 100 120 Dry Weight (mg) 0 5 10 15 20 25 30 0 20 40 60 80 100 120 Carbon (% DW) Figure 8. Callianira antarctica The seasonal relationship between total length and (A) dry weight and (B) carbon concentration for autumn (filled symbols) and winter (open symbols) 2002. Autumn : DW=(0.58)TL 1.5855 %C=( 4.8983)TL 0.1435 ; Winter: DW=(0.0179)TL 2.4861 %C=(1.0683)TL 0.6194 A Total Length (mm) B
30 Table 2. Callianira antarctica Total length, dry weight (DW), and water content as percent of the DW for autumn and winter 2002 Total Leng th Dry Weight Water Carbon Nitrogen ( mm) (mg) (%WW) ( % DW) ( % DW) Season Me di an Range Me di an Range Mean R ange Mean Range Mean Range n Autumn 46.5 3 5 .0 83. 6 2 76 150 758 96.1 95.7 97.9 8.60 7.00 12.0 1.92 1.55 2.38 8 Winter 25.5 8.5 98.0 76.6 2. 8 1366 95.5 94.2 97.0 8.35 1.41 24.9 1.80 0.30 4.43 24 Combined 34.5 8.5 98.0 132.6 2.8 1366 95.7 94.2 97.9 8. 41 1.41 24.9 1.8 3 0.30 4.43 32 There was a weak positive correlation (r = 0.31, p = 0 .05) between total length and carbon concentration (%DW) during autumn, which may be attributed to the small sample size, and a higher positive correlation (r = 0.69, p = 0.05) during winter (Fig. 8 B ). Body carbon and nitrogen content for autumn animals r anged from 7.0 to 12.0% DW and 1.6 to 2.4% DW, respectively. The range for winter carbon (1.4 to 24.9% DW) and nitrogen (0.3 to 4.4% DW) values was much broader, possibly due to the larger sample size. Geomean carbon and nitrogen (%DW) values of C. antar ctica are given in Table 2 The total body carbon and nitrogen content increased with ctenophore size for both seasons (Fig. 9 A B ). The similarity between the autumn and winter slopes of these data suggests that there was little seasonal change in body c arbon and nitrogen content. 0 10 20 30 40 50 60 70 0 500 1000 1500 Nitrogen Content (mg) 0 50 100 150 200 250 300 350 400 0 500 1000 1500 Carbon Content (mg) Figure 9. Callianira antarctica The seasonal relationship between dry weight and (A) total carbon and (B) total nitrogen for autumn (filled symbols) and winter (open symbols) 2002. Autumn: C=( 0.034 )DW 1.17 N = ( 0.016 )DW 1.0 3 ; Winter: C = ( 0.029 )DW 1.25 N=( 0.006 )DW 1.26 A B Dry We ight (mg )
31 Metabolic Rates. During winter 2002 ammonium excretion rates were measured for 15 ctenophores ranging in total length from 8.5 to 85.0 mm, with a median length of 28.0 mm. Oxygen consumption is reported for a subset of these ctenophores (n = 10), having the same range in total length but a median length of 31.0 mm (Table 3 ). Both oxygen consumption and nitrogen excretion rate per individuals increased with increasing ctenophore body size (Fig. 10 ). The regre ssion of oxygen consumption versus DW for C. antarctica yielded a value of b = 0.92 for the allometric equation: Y = aW b where Y is metabolic rate, a is the intercept, W is dry weight (mg), and b is the exponent reflecting the effect of size (Fig. 10 ). This b value is near unity, indicating that the oxygen consumption per unit mass decreased only slightly with increasing ctenophore size. The geometric (GM) regression model (linear regression of log log transformed data) for oxygen consumption as a funct ion of DW indicated a larger decrease in respiration per unit mass with increasing ctenophore size ( b = 0.80). Both the geometric and conventional regressions for oxygen consumption as a function of body carbon showed a weight dependent relationship ( b = 0.85 and 0.71, respectively) between respiration and carbon content. The weight specific oxygen consumption and ammonium excretion rates decreased with increasing size, indicating greater relative metabolic requirements for smaller ctenophores. Dry weigh t specific and carbon specific oxygen consumption rates calculated for individual C. antarctica ranged from 0.059 to 0.411 m l O 2 [mg DW] 1 h 1 and 0.471 to 7.15 m l O 2 [mg C] 1 h 1 respectively. Dry weight specific nitrogen excretion rates ranged from 0.6 0 to 31.1 g at N [g DW] 1 h 1 Geomean oxygen consumption and nitrogen excretion rates are provided in Table 3
32 Table 3. Oxygen consumption and ammonium excretion rates for Callianira antarctica and 7 other species of ctenophore Species Oxyge n consumption Ammonia excretion Temperature n l O2 ind 1 hr 1 l O2 [mg DW] 1 h 1 l O2 [mg C] 1 h 1 g at N [g DW] 1 h 1 o C Callianira antarctica 14.9 0.163 2.11 9.39 0 10,16 a Mertensia ovum nd 0.074 ( + 0.028) nd 0.24 0 59 b Mertensii dae sp. 12.1 ( + 6.30) 0.129 nd 8.11 1.6 8* b Beroe sp. 15.6 ( + 3.40) 0.025 nd 2.64 1.5 7* c Pleurobrachia pileus 1.08 1.17 0.140 0.280 nd nd 7 7.5 4 d Bolinopsis infundibulum nd 0.054 3.05 nd 5 6 10 e Bathocyroe fosteri nd 0.042 ( + 0.021) nd 0.01 0.14 9 12 49 f Mnemiopsis leidyi 30.4 0.070 0.231 4.12 13.6 0.483 1.53 10 24 40 a Percy (1988), b Ikeda & Bruce (1986), c Ikeda (1974), d Baily et al. (1994), e Youngbluth et al. (1988), f Kremer (1977) *Number of experiments performed; 2 to 5 animals each. Species Oxyge n consumption Ammonia excretion Temperature n l O2 ind 1 hr 1 l O2 [mg DW] 1 h 1 l O2 [mg C] 1 h 1 g at N [g DW] 1 h 1 o C Callianira antarctica 14.9 0.163 2.11 9.39 0 10,16 a Mertensia ovum nd 0.074 ( + 0.028) nd 0.24 0 59 b Mertensii dae sp. 12.1 ( + 6.30) 0.129 nd 8.11 1.6 8* b Beroe sp. 15.6 ( + 3.40) 0.025 nd 2.64 1.5 7* c Pleurobrachia pileus 1.08 1.17 0.140 0.280 nd nd 7 7.5 4 d Bolinopsis infundibulum nd 0.054 3.05 nd 5 6 10 e Bathocyroe fosteri nd 0.042 ( + 0.021) nd 0.01 0.14 9 12 49 f Mnemiopsis leidyi 30.4 0.070 0.231 4.12 13.6 0.483 1.53 10 24 40 a Percy (1988), b Ikeda & Bruce (1986), c Ikeda (1974), d Baily et al. (1994), e Youngbluth et al. (1988), f Kremer (1977) *Number of experiments performed; 2 to 5 animals each. 1.00 8.10 50.00 174.20 900.00 Dry Weight (mg) 0.39 0.75 2.50 4.45 7.50 15.26 25.00 50.00 75.00 Oxygen Consumption ( l 0 2 ind -1 h -1 ) 0.08 0.20 0.50 0.80 2.00 5.00 Excretion ( g-atoms N ind -1 hr -1 ) Figure 10. Callianira anta rctica The relationship between oxygen consumption (circles), ammonium excretion (squares) and dry weight. T = 0.5 o C. The equations for respiration and excretion are, respectively: Oxygen consumption = 0.237 DW 0.92 (r 2 = 0.91), and ammonium excretion = 0.051 DW 0.58 (r 2 = 0.76). The ratio of oxygen uptake to nitrogen excretion rate (atomic O:N ratio) varied from 6.37 to 138, with no relationship to ctenophore size. The geomean O:N ratio was 28.8, indicating protein oriented metabolism (Mayzaud & Cono ver 1988). Other studies on ctenophore respiration and excretion have determined that ctenophores metabolize both protein and lipids (Kremer 1977), therefore many authors assume an intermediate RQ
33 value of 0.8 when determining carbon respiration. The pro portion of each component metabolized, however, may vary significantly with season and food availability (Hoeger 1983, Kremer 1982, Percy 1988) and is further complicated by different biochemical pathways for nitrogen metabolism (Mayzaud & Conover 1988). For this reason, both lipid and protein RQ values were used to determine the amount of carbon that C. antarctica potentially needed to consume each day to support metabolism. T he range in minimum daily carbon requirements was estimated by converting the m ean oxygen consumption rate per individual to carbon respired using Gnaigers (1983) respiratory quotient (RQ) values of 0.97 for protein and 0.72 for lipid catabolism. According to Gnaiger (1983), the excretory end product determines the RQ value in prot ein catabolism: 0.97 for ammonia and 0.84 for urea. Since gelatinous zooplankton are ammonotelic, 0.97 is the appropriate RQ value for protein for this study. Based on the oxygen consumption rates for C. antarctica daily carbon requirements for small ct enophores ( = 30 mm TL) ranged from 3.6 to 190.3 m g, and for larger ctenophores (> 30 mm TL) 150.5 m g to 1.13 mg. The daily carbon requirement varied between 2.7% and 3.6% of the body total carbon for small ctenophores, and between 1.4% and 1.9% of the total body car bon for larger ctenophores. Feeding behavior. During winter 2001 and 2002, SCUBA divers observed high numbers of Callianira sp. (> 1 ctenophore m 3 ) just under the pack ice where larval krill aggregated. The ctenophores were passively drifting, mouth orie nted upwards, with their tentacles extended outward approximately ten times their body length or greater, characteristic of an ambush entangling predator (Greene 1985). Ctenophores imaged under ice during late night hours by an ROV showed similar behavior Our combined
34 observations of ctenophore predatory behavior under sea ice, and the presence of prey in the guts of ctenophores collected during late afternoon and evening tows, suggest that these ctenophores search for food continuously over a 24 h perio d. Callianira antarctica feeding behavior also was observed during experiments in winter 2002. After ctenophores were placed in 500 ml polypropylene jars containing prey, they typically proceeded to set out their tentacles by swimming in a circular patter n around the jar. Due to jar volume constraints, ctenophores were not able to release their tentacles to the extensive lengths observed in situ by divers and the ROV. ROV images also indicated that once ctenophores had extended their tentacles, they drif ted passively with currents. In jars, after one or more prey were caught in a tentacle, the ctenophores typically stopped swimming and began retracting their tentacles, drawing the prey close to their body. The actual ingestion of prey into the mouth was observed on only two occasions. In both instances, once the ctenophore had drawn the prey closer to its body, it rotated several times in the tentacular plane, effectively landing the prey held by the tentacle into its mouth. The prey, along with the po rtion of tentacle surrounding it, was moved fairly quickly from the mouth down into the stomodeum (pharynx). Digestion time. During winter 2002, 21 digestion time experiments were performed with ctenophores ranging in size from 20 to 55 mm total length. Temperature was nearly constant ( 1.0 to 1.8 o C), however type and number of prey varied with each experiment. Prey offered in experiments were the same species and sizes that were observed in ctenophore gut contents from in situ feeding, including larval and juvenile euphausiids, Euphausia superba and Thysanoessa macrura and the calanoid copepods, Calanoides acutus Calanus propinquus and Metridia gerlachii Nearly half of the experiments
35 (48%) involved digestion of one prey item and 14% involved 2 pre y items. The largest meal digested was 6 prey (n=1). In order to compare digestion rates among experiments involving different prey types, digestion times were normalized by prey DW, body carbon or body nitrogen. The DW, carbon and nitrogen values for th e prey are listed in Table 4 Table 4. Average dry weight (DW), body carbon (C) and body nitrogen (N) values for each stage of prey used in digestion time experiments Prey Stage/Sex DW ( m g) C ( m g) N ( m g) n Euphausia superba F4 514 + 27.4 160 43.6 8 Euphausia superba F5 809 + 41.6 221 60.1 10 Euphausia superba F6 1,080 + 51.0 277 75.2 26 Euphausia superba Juv/20 mm 10,309 4,264 879 33 Thysanoess a macrura Juv/11 15mm 6,478 3,279 565 5 Thysanoessa macrura Juv/15 20 mm 14,530 7,369 1039 4 Metridia gerlachi Fe 313 103 20.1 6 Calanus propinquus Fe & Ma 1,173 571 88.6 19 C = 406*DW 37.2, N =83.3*DW 1.10 (Daly submitted) C = 0.06*L 3.73 N = 0.02*L 3.57 DW = 0.7*L 3.20 (Daly unpublished) The digestion process may be described in terms of five stages based on observati ons from 18 of the winter experiments (Table 4 Fig. 11 ). The time intervals for each digestion stage are shown for each experiment in Fig. 12 Three digestion time experiments were omitted from the assessment of average stage duration, because small, li ngering portions of prey tissue or an excessive amount of food ingested resulted in exceptionally long digestion times. The digestion process began with the ingestion of prey (Stage I), and ended when most (<0.5 mm digested matter remaining) or all of the digested matter was cleared from the gut (Stage V). Callianira antarctica typically
36 digested the soft tissue first, and egested the exoskeletal remains through its mouth last. There were a few occasions, however, when soft tissue remained after all of t he exoskeletal parts were egested. For all eighteen experiments analysed, Stage II occurred within 5 h after ingestion of prey, and Stage III took place within 9 h. The duration of Stages IV and V were much more variable, ranging from 3 to 18 h and 5 to 21 h, respectively, and appeared to be highly influenced by prey type and/or carbon content (Fig. 12 ). Digestion times for all experiments (n = 21) ranged from 5 to 46 h, although in 86% of the experiments digestion was completed within 8 to 20 h, with a median time of 11.5 h. Neither total digestion time nor the hourly digestion rate as a function of ingested prey dry weight (digestion [mg prey DW] 1 h 1 ) were correlated (p = 0.5) with ctenophore size (Fig 13 ) Total digestion time was positively corre lated with ingested prey dry weight, carbon content, and nitrogen content (Fig. 14 ); the strongest correlation being with ingested carbon (r = 0.95, P < 0.05). The influence of prey type on digestion time was directly related to the elemental composition of the prey, i.e. species rich in carbon and nitrogen usually took longer to digest than species lower in elemental composition. Based on two trials, T macrura typically took 1.4 times longer to digest than a E superba of similar or larger size, probabl y because T. macrura had on average 1.7 times higher carbon content ( E. superba : 4.26 mg C; T. macrura : 7.37 mg C). However, when multiple E. superba furcilia 6 were ingested, the meal, totalling less than 2.0 mg of carbon content, took almost a half hou r longer to digest than the E. superba juvenile mentioned previously. In this case, the size of the food bolus or refractory body components may have retarded the digestion process. Even though digestion time
37 increased with the ingestion of more than one individual of the same prey type, a doubling or tripling of prey ingested did not usually correspond with a doubling or tripling in digestion time (Fig. 15 ). Table 5. Callianira antarctica. Digestion stage categories defined from winter 2002 digestion t ime experiments Stage Hours Description I -Newly ing ested prey, perfectly intact. Can usually see small amount of tentacle mass in bottom of pharynx. II 1 to 5 Losing distinguishable shape due to soft tissue digestion. III 2 to 9 Soft tissue completely separated from carapace, and usually sequestered at the bottom of the pharynx as one mass. IV 3 to 18 Only small amount (equal to or less than 1.0 mm 2 ) of digestive tissue remaining in stomodeum. Pieces of exoskeleton may or may not be completely egested. V 5 to 21 Most or all soft tissue and/or exoske letal pieces digested or egested. Figure 11. Callianira antarctica. Images of Euphausia superba in the ctenophore stomodeum during digestion Stage (from top left to bottom right) I, II,III/IV and V of digestion. Es= Euphausia superba, S=sto modeum, T=tentacle, If= infundibulum, Ex=exoskeleton, Dm=digested matter, M=mouth, Pc= pharyngeal canal. E s T If E s If Tb S E x D m If M S P c
38 0 5 10 15 20 25 48 48 50 50 55 Ctenophore Length (mm) Hours StageII StageIII StageIV StageV Copepod Krill StageII StageIII StageIV StageV Copepod Krill 20 30 35 35 Figure 12. Callianira antarctica Digestion stage intervals (h) for each experiment in relation to ctenophore length. The type, as identified in the legend, and number of prey digested are displayed for selected experiment s 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 10 20 30 40 50 60 Digestion Rate (mg DW prey/hr) 0 5 10 15 20 25 30 35 40 45 50 10 20 30 40 50 60 Total Digestion Time (h) Figure 13. Callianira antarctica. Ctenophore length versus (A) digestion time and (B) weight specific digestion rate. A B Total Length (mm)
39 y = 0.273x 2.26 r 2 = 0.91 0.0 2.0 4.0 6.0 8.0 10.0 12.0 0 10 20 30 40 50 Total Prey C (mg) B y = 0.531x 3.67 r 2 = 0.88 0.0 5.0 10.0 15.0 20.0 25.0 0 10 20 30 40 50 Prey Total Dry Weight (mg) A y = 0.041x 0.29 r 2 = 0.85 0.0 0.5 1.0 1.5 2.0 0 10 20 30 40 50 Digestion Time (h) Total Prey N (mg) C Figure 14 Callianira antarctica The relatio nship between total digestion time and (A) ingested prey dry weight, (B) total carbon, and (C) total nitrogen content.
40 0 5 10 15 20 25 30 35 40 45 50 0 2 4 6 8 Number of Prey Total Digestion Time (h) T. macrura (J) C. propinquus M. gerlachii E. superba (F) E. superba (J) Figure 15. Callianira antarctica Number of prey ingested versus total digestion time. Prey types are represented by different symb ols as indicated by the figure legend. Lipid storage. Callianira antarctica does not have oil sacs like those found in M. ovum instead lipids from prey accumulate in the stomodeum (Larson & Harbison 1989). The presence or absence, and accumulation of lipid reserves found in the stomodeum of C. antarctica collected during this study was recorded before, during and after winter digestion experiments (Fig. 16 ). Lipid was not present in the ctenophore stomodeum at the beginning of 29% of the experiments, half of which involved digestion of larval E superba and the other half involved digestion of M gerlachii and C propinquus None of the experiments with larval E. superba as prey resulted in the presence of lipid after digestion, but all of the exper iments with copepods did result in the presence of lipid. Of the experiments that began with lipid present in the ctenophore stomodeum (53%), in all cases, including those with krill larvae, the lipid droplet increased in volume with each meal, the amou nt of increase varying with prey number and type. Digestion of C
41 propinquus resulted in the largest percent increases (>100%) in lipid volume (Fig. 16 ). The percent increase from M gerlachii and euphausiid juveniles was consistently low, whereas larval E superba was highly variable, but lower than that of C. propinquus 0 50 100 150 200 (2) Es F (2) Mg (2) Tm J (1) Tm J (1) Es J (6) Es F (5) Cp (3) Cp (4) Es F (1) Mg (1) Es F & (1) Cp (1) Es F (2) Es F Prey Number and Type % Increase in Lipid Volume Figure 16. Callianira antarctica Percent increase in lipid volume measured in guts of C. antarctica after digestion of prey. Length of the ctenophore, and the number (in parenthes es) and type of prey digested are shown for each experiment. Es F = Euphausia superba Tm= Thysanoessa macrura Cp= Calanus propinquus Mg= Metridia gerlachii J=juvenile Lipid biomarker analysis A composite sample of 7 ctenophores collected in autumn (20 02) and 2 ctenophores collected in winter (2002) were analyzed for total lipid content and lipid class composition. Total lipid content in C antarctica was slightly higher in winter (4.76 0.57 % DW) than in autumn (3.51 % DW ), with p hospholipids (PL) acc ounting for more than 50 % of the total lipid content (Fig 1 7 ) F ree fatty alcohols (FALC) which are products of hydrolysis of dietary wax esters, were also detected at levels > 10% of total lipid content The l ipid class composition differed
42 seasonall y in that significant amounts of wax esters (WE) and triacylglycerols (TG) were only detected in animals from autumn Both euphausiids and copepods contained relatively large quantities of lipid =10% of dry weight, with the exception of larval krill from winter which had comparatively smaller quantities (Fig 1 7 ) WE were by far the dominant lipid class for copepods during both seasons, while TG and PL were observed in equal amounts in the adult E superba L arval E. superba from winter contained mostl y PL and smaller amounts of cholesterol and TG. Species 0 100 200 300 400 500 600 Es Ec Pa Ca Ao A CT Total lipid (mg/g DW o r for CT 10 1 mg/g DW) PL CS FFA TG WE FALC Es J F PA Mg Cp female B CT 0 500 100 200 300 400 600 PL CS FFA TG WE FALC Total lipid (mg/g DW o r for CT 10 1 mg/g DW) Species 0 100 200 300 400 500 600 Es Ec Pa Ca Ao A CT Total lipid (mg/g DW o r for CT 10 1 mg/g DW) PL CS FFA TG WE FALC PL CS FFA TG WE FALC Es J F PA Mg Cp female B CT 0 500 100 200 300 400 600 PL CS FFA TG WE FALC PL CS FFA TG WE FALC Total lipid (mg/g DW o r for CT 10 1 mg/g DW) Figure 17 Total lipid content and lipid class compositions (PL=Polar lipids, CS=Cholesterol, FFA=Free fatty acids, TG =Triacylglycerols, WE=Wax esters, FALC=Free fatty alcohols) of ctenophores and thei r potential prey sampled during autumn (A) and winter (B). CT= Callianira antarctica ES= Euphausia superba EC= Euphausia crystallorophias PA= Paraeuchaeta antarctica CA= Calanoides acutus AO= Antarctomysis ohlini MG= Metridia gerlachei CP= Calanus propinqu us Data without error bars represent the composite samples. From: Ju et al. submitted.
43 Table 6. Callianira antarctica. Fatty acid and alcohol composition (% of total fatty acid and alcohol) of ctenophores sampled during autumn and winter, 2002. From: J u et al. submitted Fall* (n=5) Winter (n=2) Acid Alcohol Acid Alcohol n Saturates 12:0 Tr 1.3.6 14:0 6.6 2.8 5.6 .8 16:0 15.5 2.2 16.3.0 18:0 1.5 0.1 1.4.1 20:0 0.1 Tr 0.1.1 0.1.1 22:0 0.2.0 Monounsaturates 14:1(n 3) Tr Tr 16:1(n 9) Tr Tr 16:1(n 7) 7.6 0.4 6.4.6 16:1(n 5) 0.2 0.2.0 16:1(n 3) Tr Tr 18:1( n 9) 14.4 0.9 10.2.9 18:1(n 7) 5.1 5.9.2 18:1(n 5) 0.4 0.5.1 20:1 + 11.6 24.7 3.5.6 38.6.2 22:1 + 1.2 68.1 0.7.1 59.1.6 24:1(n 9) 0.5.1 Polyunsaturates 16:2(n 6) 0.6 0.9.0 16:3(n 4) 0.2 Tr 16:4(n 1 ) 0.4 Tr 18:3(n 3) 0.1 0.2.1 18:4(n 3) 1.0 1.8.8 18:2 + 1.1 2.4.4 20:2(n 6) 0.2 0.7.1 20:4(n 3) 0.3 0.6.2 20:4(n 6) 0.5 0.7.1 20:5(n 3) 21.4 26.0.3 22:4(n 3) Tr 22:5(n 6) Tr 0.5.2 22:6(n 3) 9.3 12.1.9 Branched & odd chain 0.5 Tr 1.6.3 1.5.5 Total concentration (mg g 1 dry wt.) 19.3 3.8 34.3.5 6.9.5 *Composite samples were used for analysis +Indicate all isomers combined Not detected, Tr = trace amount (<0.1% of total concentration)
44 Table 7. Fatty acid (FA) and alcohol (ALC) compositions (% of total fatty acid and alcohol ) of Callianira antarctica and there potential prey. ES= Euphausia superba EC= Euphausia crystallorophias PA= Pareuchaeta antarctica CA= Calanoides acutus AO= Anarctomysis ohlini, MG = Metridia gerlachei CP= Calanus propinquus From: Ju et al. (submitted) a) Fall 2002 ES adult (n=4) EC adult (n=3) PA* (n=20) CA* (n=50) AO* (n=2) Species Acid ALC Acid ALC Acid ALC Acid ALC Acid ALC n Saturates 12:0 1.3.1 1.3 14:0 11.6.7 11.0 .7 1.7.3 66.5.8 1.1 39.0 4.5 14.8 5.1 18.5 16:0 24.4.1 5.9.1 17.9.7 5.9.1 2.9 25.1 10.1 20.0 17.0 24.3 18:0 1.4.2 1.1.1 0.1 0.7 0.6 0.9 1.1 0.9 20:0 Tr Tr 0.2 0.2 0.4 0.1 0.6 22:0 Tr 0.2 Monounsatu rates 14:1(n 3) 0.1.0 Tr 0.4 0.4 Tr 0.1 0.1 0.1 16:1(n 9) 0.1.0 0.1.0 Tr Tr 0.1 16:1(n 7) 7.2.7 6.0.7 1.7.2 27.0 4.9 9.3 3.7 9.1 3.1 16:1(n 5) 0.2.0 0.1.0 0.2 0.3 0.2 16:1(n 3) 0.1.0 0.1.0 Tr Tr 18:1(n 9) 13.2.4 76.5. 5 38.6.0 Tr 27.0 7.3 6.2 5.3 16.9 10.5 18:1(n 7) 7.6.4 13.4.5 2.5 Tr 4.6 Tr 6.4 Tr 18:1(n 5) 0.1.0 0.1.0 0.7 1.1 0.7 20:1 + 1.5.1 8.4 12.9 10.3 44.3 6.7 24.3 22:1 + 0.8.1 2.5.9 1.2 6.1 9.2 9.7 13.7 24:1(n 9) 0.6 2.3 Polyunsaturates 16:2(n 6) 0.9.1 1.0.1 0.5 0.9 0.6 16:3(n 4) 0.2.0 0.1.0 0.6 1.1 0.1 16:4(n 1) 0.7.0 0.1.0 1.7 4.5 0.3 18:3(n 3 ) 0.1.0 0.1.0 0.1 0.1 0.1 18:4(n 3) 1.2.3 0.9.1 1.9 2.7 0.6 18:2 + 0.7.0 1.6.2 1.0 1.3 0.9 20:2(n 6) Tr Tr 0.2 20:4(n 3) 0.2.1 0.1.0 0.2 0.7 1.3 20:4(n 6) 1.1 0.2 0.2 20:5(n 3) 21.3.2 13.2.2 13.6 20.0 15.1 22:4(n 3) 0.5 1.4 0.4 22:5(n 6) Tr 0.3 22:6(n 3) 3.9.5 0.9.2 6.2 7.3 11.4 Branched & odd chain 2.4.1 1.7.1 1.5.3 1.9 3.0 2.6 1.0 1.7 1. 5 Total concentration (mg g 1 dry wt.) 236.2 .8 0.2.1 217.7 .5 79.5.6 222.9 118.4 190.7 148.0 56.9 8.0 Continued on the next page
45 Table 7. ( continued ) b) Winter 2002 ES adult (n=6) ES juvenile (n=4) ES furciliae* (n=4) PA* (n=10) MG* (n=20) CP female* (n=10) Species Acid Acid Ac id ALC Acid ALC Acid ALC Acid n Saturates 12:0 1.9.3 3.2 2.2 1.3 0.9 0.9 14:0 13.4.9 11.6.8 3.2 37.6 1.4 32.3 0.5 37.5 2.6 16:0 24.5.9 25.1.4 19.3 35.4 2.8 33.2 5.6 34.1 13.1 18:0 1.3.2 1.7.3 1.0 2.5 0.3 1.6 0.4 2.8 1.0 2 0:0 Tr Tr Tr 0.3 Tr Tr Tr Tr 0.5 22:0 0.1 Tr Tr 0.2 Monounsaturates 14:1(n 3) 0.2.0 Tr Tr 0.4 Tr 0.2 Tr 16:1(n 9) Tr Tr Tr 0.1 Tr Tr 16:1(n 7) 9.5.2 9.4.2 4.3 0.7 26.4 3.1 9.4 3.7 4.5 16:1(n 5) 0.3.2 0. 3.1 0.1 0.5 0.2 1.0 0.1 0.9 0.2 16:1(n 3) Tr 0.1.0 0.1 0.4 Tr 1.0 Tr 0.9 Tr 18:1(n 9) 13.2.8 12.1.7 10.5 1.4 33.9 6.4 25.4 8.9 1.6 18:1(n 7) 7.7.2 6.8.6 8.5 2.7 1.9 3.1 1.2 1.4 18:1(n 5) 0.1.1 0.2.0 0.3 0.7 0.4 0.2 2.0 20:1 + 1 .3.5 0.9.0 1.2 3.8 3.3 5.7 12.0 0.8 4.6 22:1 + 0.6.4 11.8 0.2 4.2 0.3 45.6 24:1(n 9) 1.6 1.7 2.3 Polyunsaturates 16:2(n 6) 1.0.2 1.4.1 0.8 0.6 0.8 0.5 16:3(n 4) 0.2.0 0.3.1 0.2 0.2 0.3 0. 1 16:4(n 1) 0.7.1 1.3.3 0.5 0.4 0.7 Tr 18:3(n 3) 0.3.0 0.3.1 0.2 0.2 0.2 Tr 18:4(n 3) 1.7.4 2.7.6 1.6 3.0 2.7 0.4 18:2 + 1.8.7 1.7.6 1.9 0.7 2.0 0.4 3.2 0.4 0.7 20:2(n 6) Tr 0.1 Tr 0.2 Tr Tr 20:4(n 3) 0.3.2 Tr 0.2 0.3 0.6 0.9 20:4(n 6) 0.3.3 0.2.1 1.0 0.2 0.3 Tr 20:5(n 3) 13.6.1 14.5.3 24.4 9.4 18.4 5.7 22:4(n 3) 0.2 22:5(n 6) 0.2.1 Tr 0.7 1.2 4.9 22:6(n 3) 4.0.2 2.6.6 12.6 7.6 12.6 0.6 Branched & odd chain 3.8.8 8.1 4.7 5.1 1.3 5.8 1.1 6.4 2.3 Total concentration (mg g 1 dry wt.) 223.4 .0 210.0.0 59.5 2.5 188.4 93.7 108.1 55.6 194.5 None or only trace amounts (<0.1 mg g 1 dry wt.) of fatty alcohols (20:1 + ) were found in ES adult, ES juvenile, and CP. *Composite samples were used for analysis. +I ndicate all isomers combined. Not detected. Tr = trace amount (<0.1% of total concentration).
46 a) Fall 2002 S terols CT* (n=5) ES adult (n=4) EC adult (n=3) PA* (n=20) CA* (n=50) AO* (n=2) 24 norcholesta 5,22 dien 3 b ol (C 26 D 5,22 ) 0.4 13.1 9.6 0.2 cholesta 5,22 dien 3 b ol (C 27 D 5,22 ) 2.7 0.5.1 7.7 14.3 1.0 5 a cholest 22 en 3 b ol 0.4 1.9 1.8 Cholest 5 en 3 b ol (Cholesterol) 73.0 71.3.9 55.7.0 46.8 36.3 88.2 5 a cholestan 3 b ol (Cholestanol) 0.8 3.6.2 1.5 Cholesta 5,24 dien 3 b ol (C 27 D 5,24 ) 22.0 24.6.9 28.4.2 30.5 25.6 5.7 Cholest 7 en 3 b ol (C 27 D 7 ) 0.1 15.9.3 14.1 1.7 24 methylcholesta 5,24(28) dien 3 b ol (C 28 D 24(28) ) 0.6 24 methylcholest 5 en 3 b ol (C 28 D 5 ) 0.1 Total sterols (mg g 1 dry wt.) 0.3 1.8.7 2.5.0 2.1 1.6 4.6 b) Winter 2002 S terols CT (n=2) ES adult (n=6) ES juvenile (n=4) ES furciliae* (n=4) PA* (n=10) MG* (n=20) CP female* (n=10) 24 norcholesta 5,22 dien 3 b ol (C 26 D 5,22 ) 0.3.2 0.6.6 1.6.4 0.4 6.2 2.1 cholesta 5,22 dien 3 b ol (C 27 D 5,22 ) 1.7 0.4 0.8.2 0.8.1 4.9 12.8 12.7 17.9 5 a cholest 22 en 3 b ol 0.1.1 Tr Tr Cholest 5 en 3 b ol (Cholesterol) 80.7.3 82.3.8 85.4.1 78.6 71.8 61.8 37.4 5 a cholestan 3 b ol (Cho lestanol) 1.0.6 0.6.8 Tr 2.4 9.5 3.7 Cholesta 5,24 dien 3 b ol (C 27 D 5,24 ) 15.9.4 15.7.8 12.1.8 13.7 5.3 15.7 32.8 Cholest 7 en 3 b ol (C 27 D 7 ) 9.1 24 methylcholesta 5 ,24(28) dien 3 b ol (C 28 D 24(28) ) 0.2.0 Tr 0.7 0.7 24 methylcholest 5 en 3 b ol (C 28 D 5 ) Tr Total sterols (mg g 1 dry wt.) 1.2.2 2.8.2 1.9.4 4.6 4.8 0.4 0.7 *Composite samples were used for analys is. Not detected. Tr = trace amount (<0.1% of total concentration). Tab le 8. S terol composition (% total concentration) of Callianira antarctica and their potential prey CT= Callianira antarctica ES= Euphausia superba EC= Euphausia crystallorophias PA= Pareuchaeta antarctica CA= Calanoides acutus AO= Anarct omysis ohlini, MG = Metridia gerachei CP= Calanus propinquus From : Ju et al. (submitted)
47 The individual lipid compositions ( i.e., FA alcohols and sterols) of C antarctica were relatively constant between seasons Fatty acid (FA) and alcohol composition of ctenophores sampled in autumn and winter are shown in Table 6 and results for their prey shown in Table 7 T he total FA concentration in winter ( 34.3 mg [ g DW ] 1 ) was substantially higher than the autumn concent ration (19.3 mg [ g DW] 1 ). C allianira antarctica contain ed a wide range of FA ranging from C 12 to C 24 however t he 20:5(n 3) 16:0 and 18:1(n 9) species were the primary FA observed in ctenophores These fatty acids were also dominant in both copepods and krill for both sampling seasons Small amounts of monounsaturated fatty alcohols, particularly 20 : 1 and 22 : 1 were also found in both autumn and winter ctenophores Euphausia superba furcilia and the copepod Paraeuchaeta antarctica were the only pr ey item s to contain these alcohols at noticeable levels. The sterol concentration in ctenophores also increased between autumn and winter from 0.3 to 1. 2 0.2% DW, respectively, though low sterol levels were observed overall (Table 8 ) The sterol distri butions of ctenophores were similar to those for krill, particularly E. superba furcilia. The two dominant sterols found in ctenophores cholesterol and choleta 5, 24 dienol (C 27 D 5,24 ), were found in similar concentrations in all prey species. Gut content s. The gut contents of C antarctica during winter 2001 ( n = 20 ), autumn 2002 ( n = 43 ) and winter 2002 ( n = 82 ) were examined to determine in situ feeding. For all seasons, 4 0% or more of ctenophore guts did contain prey remains (excluding lipids) and o f those with digested matter, very few contained recognizable prey in Stages I or II of digestion. A majority of the digested matter found in gut contents f rom all three sampling periods consisted of small portions of small clumps of
48 light colored gummy material typical of Stage IV digestion. Diet items in varying stages of digestion indicated that ctenophores ingested multiple overlapping meals. During winter 2001, 20% of the guts were completely empty, 30% had lipid only, and 50% of the ctenophores ha d digested matter in their guts (Fig. 1 8 ). Thirty five percent of the digested matter was recognizable prey. Euphausiid furcilia made up the majority of recognizable prey (82.6%), and copepods and amphipods (e.g., Primno macropa ) both contributed 8.7%. C alanus propinquus which was the only identified species of copepod, made up 4% of the copepods (Fig. 1 9 ). During autumn 2002, 20.5% of the guts were completely empty, 20.5% of the ctenophores had lipid only, and 59.1% had digested matter of some form in their guts (Fig. 1 8 ). Only 16% of the digested matter was recognizable prey, consisting mostly of copepods (39% C acutus 28% C. propinquus and 22% unidentified remains of copepods), and few euphausiid furcilia (11% of recognizable prey; Fig. 1 9 ). Altho ugh a larger number of ctenophores were examined for gut content analysis during winter 2002, the results were similar to those from the two previous seasons. Of the 82 ctenophores examined, 28.1% of the guts were completely empty, 26.8% had lipid only, a nd 45.1% had some form of digested matter (Fig. 1 8 ). Only 11% of the digested matter found in the guts was recognizable prey remains, the rest typically consisted of material in Stages III and IV of digestion. The recognizable prey consisted of euphausii ds and copepods at 38.5% and 61.5%, respectively. M. gerlachii and C. acutus were the only species of copepod that could be identified (8% of recognized prey each; Fig. 1 9 ). Copepods that were too far into the digestion process to be identified to genera made up 31% of recognizable prey.
49 Lipid Only 30% Empty 20% RD prey 35% URD digested matter 15% URD digested matter 42% RD prey 16% Lipid Only 21% Empty 21% Lipid only 27% Empty 28% URD digested matter 34% RD prey 11% Figure 1 8 Callianira antarctica Gut contents of ctenophores collected during three seasons ; from left to right: winter 2001 (n = 20), autumn 2002 (n = 43), winter 2002 (n = 82). RD=Recognized, URD=Unrecognized. 0% 20% 40% 60% 80% 100% Unidentified Euphausiids Unidentified Copepods C. acutus C. propinquus M. gerlachi Amphipod Percentage of Gut Contents Winter 2001 Fall 2002 Winter 2002 Figure 19. Callianira antarctica Prey type making up the recognizable prey portion of gut contents from ctenophores collected during three seasons: winter 2001 (n=23), autumn 2002 (n=18), winter 2002 (n=13).
50 DISCUSSION Chemical composition. Call ianira antarctica did not undergo a large seasonal change in elemental composition between autumn and winter, but there was greater variability in the carbon and nitrogen content of winter ctenophores than in autumn animals, particularly for larger individ uals. These findings may have been an artifact of the small sample sizes, especially for autumn. Variability in ctenophore body carbon has been related to prey availability (Kremer 1982, Reeve et al. 1989), which was shown to largely decrease between aut umn and winter in our study area (Ashjian et al., in press). Therefore patchy distribution of prey during winter may account for the variability in the winter samples. Another source of variability in the elemental composition could be due to the collect ion method. Given that the body carbon in ctenophores is unevenly distributed among the tentacles, gut wall and comb rows (Reeve et al. 1989), loss of portions of the tentacles on some individuals during net collection would contribute to differences in c arbon content. However during winter, gentler collection with SCUBA and drift nets in addition to net tows allowed for retrieval of ctenophores in excellent condition. In addition, regardless of the collection method, great effort was made to ensure th at only complete animals in excellent condition were saved for chemical analysis, which would greatly reduce this source of error. Because the geomean carbon and nitrogen values for both seasons were similar to each other (autumn: 8.6 and 1.80% DW, respec tively; winter: 8.35 and 1.92% DW, respectively) averages of the pooled data are used in the discussion below. Callianira antarctica has a high water content and low organic mass, which is characteristic of all ctenophores and other gelatinous zooplankto n (Percy & Fife 1981,
51 Hoeger 1983, Clarke et al. 1992). Because of the high water content and the fact that conventional drying methods do not completely free gelatinous tissue of its bound moisture (Larson 1986, Clarke et al. 1992), the measured dry weig hts may be overestimated. The methodology used in this study, however, is similar to that used by other gelatinous zooplankton investigators; therefore, the data may be compared to other published values. The mean DW for C antarctica (4.2% WW) is within the range (1 to 7%) reported for other ctenophores (Kremer 1977, Hoeger 1983, Martinussen & Bmstedt 1999), and closely resembles values given for other polar cydippids, such as Pleurobrachia sp. (4.4%) from the Antarctic (Clarke et al. 1992), and P. pile us (4.0%) and M. ovum (4.5 to 4.9%) from the Arctic (Hoeger 1983, Percy 1988). The 78.9% ash content for C. antarctica is slightly higher than the ash content reported for Pleurobrachia sp. (68.3%) from the Southern Ocean (Clarke et al. 1992), and is cons istent with the high ash content values typical of gelatinous zooplankton due to the considerable inorganic salt content of the dry mass (Ikeda 1971, Hoeger 1983, Kremer et al. 1986a, Larson 1986). Body carbon and nitrogen contents of C antarctica are l ow in comparison with non gelatinous marine zooplankton, but are similar to other ctenophores from polar regions, and higher than temperate and tropical species. The geomean carbon and nitrogen values, 8.41 and 1.83% DW respectively, for C. antarctica are four to five times lower than most non gelatinous species of zooplankton from the Southern Ocean (Donnelly et al. 1994), but are only slightly lower than values for Beroe sp. (9.51 and 2.22% DW; Clarke et al. 1992) and Mertensiidae sp. (11.2 and 2.4%; Ike da & Bruce 1986), and two fold higher than those for Pleurobrachia sp. (4.11 and 0.74% DW; Clarke et al. 1992)
52 from the Southern Ocean. The mean carbon value for C. antarctica is also more than double the value for P. pileus (3.4%) from the Arctic, but si milar to that for Beroe gracilis (7.2%; Hoeger 1983). Carbon and nitrogen concentrations in C. antarctica are also more than four times higher than those in epipelagic ctenophores from temperate and tropical regions (reviewed in Youngbluth et al. 1988). The elevated carbon levels in C. antarctica in comparison to temperate and tropical ctenophores are expected, as high latitude species typically have higher carbon content than similar species in lower latitudes (Ikeda 1977). The more than two fold differ ence in carbon and nitrogen concentrations between C. antarctica and Pleurobrachia sp. from both the Arctic and Antarctic is not as easily explained. Both groups are moderately robust species of cydippids that, for the most part, are able to withstand net collection techniques that severely damage more delicate ctenophores. Callianira antarctica is a larger species of ctenophore (Hoeger 1983, OSullivan 1986), however, that may structurally require a higher carbon and nitrogen concentration. Without furt her morphometric analysis of the two species we cannot account for the difference in elemental composition. Metabolic rates. Callianira antarctica metabolic rates were very similar to those of Mertensiid ctenophores from the Antarctic, but were higher th an those measured for M. ovum from the Arctic (Table 2). The geomean weight specific oxygen consumption rate for C. antarctica (0.163 l O 2 [mg DW] 1 h 1 ) is only slightly higher than the mean value for Mertensiidae sp. (0.129 l O 2 [mg DW] 1 h 1 ) mea sured at 1.6 o C during austral spring in the Prydz Bay region of the Antarctic (Ikeda and Bruce 1986). The geomean nitrogen excretion rates from these same studies are very close as well: 9.39 g at N [mg DW] 1 h 1 for C. antarctica vs. 8.11 g at N [mg DW] 1 h 1 for Mertensiidea sp. The wet
53 and dry weights of C. antarctica and Mertensiidae in the experiments were nearly identical, and the temperatures were similar despite the difference in season. In contrast, the geomean weight specific oxygen consum ption rate for C. antarctica was more than twice the mean rate measured for the Arctic cydippid M. ovum (0.074 0.028 l O 2 [mg DW] 1 h 1), and C. antarctica s geomean nitrogen excretion rate was almost two orders of magnitude greater than the mean value for M. ovum (0.24 g at N [mg DW] 1 h 1 ) during winter (Percy 1988). The season of sampling, temperature, size range and mean DW (%WW) for C. antarctica were all similar to that of M. ovum, however, the median total wet and dry weight (mg) for C. antarctica was only a quarter of mean wet and dry weight (mg) for M. ovum The larger mass of M. ovum may account for the l ower specific metabolic rate in comparison to C. antarctica as larger animals tend to have lower weight specific respiration and nitrogen excretion rates (Ikeda 1970, 1974 & 1985). The metabolic rates of ctenophores are also significantly affected by fe eding history (Kremer 1982). Percy (1988) attributed a 30% decline in M. ovum respiration rates between summer and winter to a substantial decrease in seasonal abundance of prey. Adult M. ovum occurs in the upper 30 m of the water column in Frobisher Bay in the Canadian eastern Arctic throughout the year, but were not collected in nets set just below the sea ice during winter, and therefore may not take advantage of the zooplankton community below the undersurface of the ice (Percy 1989). In contrast, du ring our study, diver observ ations and gut content analysis proved C. antarctica to be an effective predator on larval and juvenile krill associated with the undersurface of sea ice. Exploitation of this winter food source may provide a predatory advantag e and contribute
54 to C. antarcticas higher winter metabolic rate compared with that of M. ovum The disparity in metabolic rates between C. antarctica and M. ovum also can be considered in a evolutionary context by application to the hypothesis that the A rctic is a younger ecosystem and its species may not be fully adapted to the colder waters; therefore, the metabolic rates of Arctic species will be lower than those species from the Antarctic (Holeton 1974, Clarke 198 4 ; as referenced in Ikeda et al. 200 0). While this application may be interesting, and possibly valid, the hypothesis has yet to be substantiated (Ikeda 1989) The geomean weight specific oxygen consumption rate of C antarctica is at the lower end of the range given for P. pileus (0.140 0. 280 l O 2 [mg DW] 1 h 1 ; Ikeda 1974) and other ctenophores from temperate and tropical regions (0.129 0.848 l O 2 [mg DW] 1 h 1 ; as referenced in Percy 1988). These findings are consistent with the general rule that oxygen consumption for polar specie s of zooplankton is low in comparison to temperate and tropical species (Ikeda 1970 & 1974, Clarke & Peck 1991), due in large part to the differences in habitat temperature (Ikeda 1985). If a Q 10 of 2 is assumed (Prosser 1961, Percy 1988), at 10 o C C. anta rctica would respire at a rate (0.326 l O 2 [mg DW] 1 h 1 ) slightly greater than rates measured for Pleurobrachia spp. at similar temperatures (0.26 0.28 O 2 [mg DW] 1 h 1 at 7.5 13 o C; Hirota 1972, Ikeda 1974), indicating cold adaptation in C. antarctica The linear regression of log log tr ansformed data (GM) for oxygen consumption in terms of dry weight and carbon content indicated a weight dependent respiration for C. antarctica Values of b indicating weight dependent respiration in the range of 0.6 to 0.9 are characteristic of ctenoph ores and marine zooplankton in general (Ikeda 1974,
55 Ikeda & Mitchell 1982, Kremer et al. 1986b, Bailey et al. 1994, Percy 1988, Ikeda et al. 2000). However values ranging from 0.9 to 1.28, indicative of weight independent respiration, have been reported f or ctenophore species such as Mnemiopsis leidyi (Kremer 1977), Mnemiopsis mccradyi (Kremer 1982) and Bathyocyroe fosteri (Youngbluth et al.1988). Bailey et al. (1994) attributed the variability in b values among species of ctenophores to methodological treatments as well as low sample sizes in the studies. Further experiments with larger samples sizes are necessary in order to confirm C. antarctica s metab o lic relationship to size. Maintenance carbon rations and body turnover. Sm aller C. antarctica req uired a higher carbon specific maintenance ration to support metabolic processes than larger ctenophores during winter. The minimum amount of carbon that C. antarctica needed to ingest daily during winter was calculated to be 3.61 g to 0.190 mg for small ctenophores (average 2.7% to 3.6% total body carbon), and 0.151 to 1.13 mg for larger ctenophores (average 1.4% to 1.9% total body carbon). The higher maintenance ration for smaller C. antarctica was due to having higher weight specific respiration rates combined with a lower carbon content on a per unit weight basis. The mean daily maintenance ration (1.5% body C d 1 ; Ikeda & Bruce 1986) for large Mertensiidae from the Antarctic in early summer is within the range of average values for large C. antarcti ca The range in maintenance rations reported here are greater than that estimated for M. ovum of a similar size range from the Arctic during winter (ca. 0.2 to 1.5% body C d 1 RQ: 0.8; Siferd & Conover 1992), but smaller than that reported for mesopela gic and epipelagic ctenophores (5 to 11% body C d 1 ) from tropical waters between spring and autumn (Kremer et al. 1986b, Youngbluth et al. 1988).
56 Even if we assume a very conservative assimilation efficiency of 70% (Reeve et al. 1978), the maximum daily carbon requirement to support metabolism for small C antarctica during winter would be satisfied with the ingestion of one larval (F6) E superba one adult C propinquus or two M gerlachii Larger ctenophores (>20 mm) would need to ingest up to 6 lar val (F6) E. superba 16 M. gerlachii 3 C. propinquus or 1 juvenile E. superba or T macrura each day. A verage winter digestion times (e.g., 10.0 and 16.5 hours for prey items under 1.0 and 2.0 mg C, respectively) would allow for multiple meals each day, suggest ing that C. antarctica may have been able to meet, and possibly exceed, the maintenance daily carbon requirement. In gestion rate experiments with C. antarctica in austral autumn indicated that at prey concentrations of ca 40 g C 1 l 1 the minimum daily ration was equivalent to 17 % of body carbon ( Scolardi et. al submitted ) I ngestion rates for winter are not likely to be as high as the autumn rates due to reduced temperatures and prey concentration s yet a reduction in ingestion rates as large as one half the original would still bring in sufficient food to meet minimum maintenance rations although very little to none will be left for allocation to growth and reproduction. Feeding ecology: experimental. Sluggish digestion rates may be the limitin g factor in the amount of carbon C antarctica can process in excess to the minimum maintenance ration on a daily basis. The mean winter digestion time for C. antarctica (11.5 h) was substantially longer than values reported for temperate and tropical cte nophores (Fig. 20 ; range 0.2 5.8 h, T = 5 26C). Copepods in tropical waters (25 27 o C) are typically digested in less than 3 hours (Reeve 1980, Kremer et al. 1986a, Larson 1987b), whereas C. antarctica took 9 to 12 h to digest a single copepod in ou r study. Unfortunately there
57 are few investigations on digestion processes of polar ctenophores for comparison. Mertensia ovum from the Canadian High Arctic digested <1 mm to 6 mm copepods significantly faster (1.5 to 4 h; Siferd & Conover 1992) than C. antarctica The M. ovum rate is shown in Fig 20 as a comparison with the other published rates, but was not included in the functional relation between digestion rate and temperature because temperatures in the experimental aquaria ( = 1.5 o C) were higher t han in situ winter temperatures, which would have resulted in more rapid digestion of prey. Also, the authors did not include egestion of the indigestible exoskeleton in the gut evacuation time, which may have shortened the actual digestion time. For all other published digestion rates, temperature explained almost 50% of variability in the digestion time of different prey types ranging from fish eggs to euphausiid larvae (Fig. 20 ). y = 9.40e -0.096x r 2 = 0.50 0 2 4 6 8 10 12 -5 0 5 10 15 20 25 30 Water Temperature (C) Digestion Time (h) Frank 1986 Reeve 1980 Larson 1987a Larson 1987b Monteleone & Duguay 1988 Sullivan&Reeve 1982 Reeve & Walter 1978 Fall Winter X Figure 20. Relationship between digestion time and incubation temper ature for ctenophores. Data from: Reeve and Walter (1978), Reeve (1980), Sullivan & Reeve (1982), Frank (1986), Larson (1987a,b), Monteleone and Duguay (1988) and this study. Callianira antarctica rates designated by triangle; the data designated by the X (Siferd & Conover 1992), was not included in the functional relationship; see explanation in text.
58 Winter digestion times for C antarctica were independent of ctenophore size, but highly correlated with prey number. The influence of prey number was tw o fold: digestion time lengthened with the increasing amount of prey carbon consumed, and was further retarded by the size of the food bolus and/or accumulating chitineous exoskeletons in the gastrovascular cavity Other studies have shown a lack of corre lation between digestion time and ctenophore size, but a positive correlation with prey number (Martinussen & Bmstedt 1999, Larson 1987b). However, Martinussen & Bmstedt (1999) also found that that digestion time in two species of scyphomedusa decreased with increased medusa diameter, but increased with prey number. In addition, Reeve (1980) reported that the mean digestion time of Mnemiopsis mccradyi decreased from two to one h after it reached > 4 mm in length. However, this decrease was attributed t o a change in the selection of food at this size; after this adjustment, the digestion time remained consistent through 13 mm. Reeve (1980) observed an increase in digestion time in M. mccradyi with increasing prey number as well. Prey type also was a s ignificant factor in influencing winter digestion time. The influence of prey type is a function of the prey tissue structure, which governs the digestion process (Hirota 1974, Larson 1987a, Martinussen & Bmstedt 1999). For C antarctica prey with grea ter lipid or carbon content, such as C propinquus and T macrura took longer to digest than other prey of similar size. That the digestion rate did not increase linearly with increasing ingested prey carbon indicates some level of enzymatic mediation is involved. The remaining variability in digestion times that cannot be explained by prey number or prey type may, therefore, reflect differences in enzyme function (Hirota 1974).
59 Callianira antarctica assimilation efficiencies appeared to be very high si nce they egested little other than clear pieces of disarticulated exoskeleton during digestion experiments. The major organic component of exoskeletons is chitin, which on average is 4.6% DW in copepods (Bmstedt 1986), and 4.0% DW in E superba (Raymont 1983); hence, carbon assimilation efficiencies could be >90%. The accumulation of lipid droplets in the stomodeum of C. antarctica suggests, however, that some portion of prey carbon is not immediately assimilated. In his review of lipid composition of A ntarctic zooplankton, Clarke (1984) found accumulation of wax ester (storage lipid) droplets in every ctenophore, tentatively identified as Pleurobrachia sp., that he examined. Arctic gelatinous zooplankton are known to store lipid after feeding on copepo ds, which has been suggested as a survival strategy during times of low food availability (Percy 1988). Percy (1988) found that the ratio of oxygen consumed to nitrogen excreted (O:N) in M. ovum increased in winter, suggesting a shift towards lipid based metabolism fuelled by increased lipid reserves accumulated from their lipid rich prey (copepods). The results obtained from this study, however, indicate that C antarctica lipid stores are not used as a n over wintering strategy. Ctenophores in autumn ha d small concentrations of wax esters (storage lipid) and triacylglycerols (short term energy reserves) but zero levels of this lipid during winter The total lipid concentration actually increased in C. antarctica from autumn to winter but was mostly du e to an enrichment in structural lipids (PO) In addition excretion m easurements for C. antarctia resulted in a geomean O:N ratio that was more indicati ve of protein than lipid oriented metabolism Furthermore, the possible degrowth of some portion of the ctenophore population during winter, as suggested by
60 the length frequency distribution s f r o m autumn and winter, does not support the theory of lipid accumulations being used as an over wintering strategy by C. antarctica. Accumulations of lipids in the gut of ctenophores may be used to infer ctenophore diets Lipid class analyses of these accumulations were not performed for this study however literature on lipid deposits in the stomodeum of Antarctic ctenophores (Clarke 1984, Larson & Harbison 19 89) indicates that these accumulations consist ed mostly of WE or TG. Due to the fact that lipid in Antarctic copepods are largely comprised of WE or TG (Clarke 1984, Hagen et al. 1993) whereas the lipid content of Antarctic euphausiids is more variable implies that these sequestered lipids are mostly from the digestion of copepods For example, copepodite stage V C propinquus has a reported lipid content of 25 47% DW stored largely as WE (Conover & Huntley 1991) whereas i mmature E superba in the WAP region had generally low levels of lipids (12 20% DW) stored primarily as TG ( Stbing et al. 2003, Ju & Harvey in press). L ipid content analysis of l arval E. superba from this study had low lipid concentration, with no indication of WE However, T macrura typically has a total lipid content of >50% DW also predominantly stored as WE ( Clarke 1984, Falk Petersen et al. 1999) and therefore may also be a source of these lipid stores Copepods as the primary source for the lipid accumulations is fur ther supported by the digestion rate experiments, where differences in the quantity and type of lipids found in prey used in winter experiments resulted in varying accumulations of lipid in the stomodeum of C. antarctica with the largest amount occurring after the digestion of copepods, particularly C propinquus rather than the digestion of larval euphausiids. Therefore, of the 20 to 30% of the ctenophores examined for gut contents that contained
61 only lipid droplets, with no other evidence of prey in th eir gut, it is likely that they had previously ingested copepods. These results, however do not exclude krill as a possible prey source. Observations of lipid in the guts of ctenophores also do not necessarily indicate recent feeding either, as Larson & Harbison (1989) noted that accumulated lipids in the gut of C antarctia from the Ross Sea during summer remained there for more than two weeks. The results of the lipid biomarker analyses allow us to make more definitive connections between ctenophor e and their prey. The observed low l ipid concentrations (2 7% of dry weight) dominated by PO in C. antarctica is consistent with results reported for other Antarctic ctenophores ( Clarke 1984, Nelson et al. 2000) Wax esters and TG were detected in C. ant arctica in autumn, but not in winter. The presence of these two neutral lipid classes may reflect active feeding on lipid rich copepods in autumn, and their absence in winter may suggests reduced feeding activity (Ju et al. submitted) Major fatty acids (16:0, 16:1(n 7), 18:1(n 9), and 20:5(n 3)) observed in ctenophores were also found in larval and adult krill. S ignificant amounts of the MUFA 20 : 1 and 22 : 1 were found in ctenophores which are known to be important component s of wax esters in calanoid co pepods a lthough E. superba furcilia in this study also contained these alcohols at noticeable levels Cholest 5,22 dien 3 b ol (C 27 D 5,22 ) the major sterol in the Antarctic ice diatom Nitzschia cylindrus (Nichols et al. 1986 ; as referenced in Ju et al. su bmitted ) accounted for a significant fraction of the total sterols in copepods and larval krill. The appearance of this sterol in ctenophores indicates that copepods and larval krill may be a significant food source for C. antarctica during winter.
62 Lipi d compositions in C. antarctica showed similarities with both copepods and adult krill for both seasons and larval krill in winter W hile adult krill were considered in the analysis, it is questionable that C. antarctica could successfully capture and ing est adult krill, although the breaking stren gth of ctenophore tentacles suggest s th at th e tentacles of large C. antarctica could successfully hand le prey as long as 4 cm (Matsumoto pers. comm.) The absence of copepod associated WE in winter animals does s uggest a possible shift towards larval kri ll as a major source of food, which was strongly supported by gut contents analysis from the first winter, but to a lesser degree in winter 2002. Feeding ecology: in situ Recognizable prey items from gut contents indicated that C antarctica were preying predominantly on larval euphausiids during winter 2001, predominantly on copepods during autumn 2002, and on larval euphausiids and copepods during winter 2002. Although there is some level of selectivity in prey capture with ambush predators, as they tend to catch relatively large, fast moving prey (Greene et al. 1986, Larson 1987c, Madin 1988, Purcell 1997), tentaculate ctenophores are opportunistic feeders, and as a result their gut contents reflect in situ pre y concentrations and compositions (Frank 1986, Siferd & Conover 1992). Diver and ROV observations under sea ice and results from net tows (Daly in press; Ashijian et al. in press) over three sampling periods support what was seen in the gut contents: larv al E superba concentrations were highest during winter 2001, lowest during autumn 2002, and variable in winter 2002. Although overall prey abundance varied between season and years, 40 5 5 % of the gut contents for all three seasons did not contain any digested material neither
63 recognized nor unrecognized This seasonal consistency contradicts the findings of Frank (1986) who concluded that the feeding incidence of P. pileus off southwestern Nova Scotia in the spring, which varied from an average of 4 6% to 84%, paralleled the total zooplankton biomass available to ctenophores. Contrary to this frequencies of empty guts reported for M. ovum (52% to 70%) from the Arctic (Siferd & Conover 1992), where prey densities are highly seasonal, compared to thos e for Bolinopsis vitrea (40 80%) from Bimini Harbor (Kremer et al. 1986a), which has low, but steady prey densities year round show a similar range in feeding inci dence despite differences in seasonal variability of total prey biomass This comparison indicates that factors other than total zooplankton biomass such as prey patchiness, may significantly influence feeding in ctenophores The results of this study suggest that C. antarctica overcome decreased prey concentrations and increased prey patchi ness by exploiting larval krill aggregations under the sea ice. The important role of larval krill aggregations under sea ice in the feeding ecology of C. antarctica implies that the success of larval krill could be directly tied to the success of ctenoph ores during winter. While experimental digestion rates and information on ingestion rates indicate that C antarctica are capable of meeting their metabolic requirements, t he question still remains : do in situ observations indicate that C antarctica is su ccessfully feeding? This is not immediately obvious, as f eeding incidences of ca 50 % could mean half of the ctenophores are fed or half are starved. We must give success a quantitative value, such as minimum daily ration Assuming that a large ctenophor e ingests its minimum daily carbon requirement (1.13 mg C) in one sitting, then the equation in F ig 14 B can be used to calculate the time of digestion. If it takes a total of 12.4 hours for the ctenophore to
64 digest its minimum carbon requirement for that day, then it can be said that there is a 52% chance that this ctenophore will be caught with food in its gut This is a noticeably good match with the actual feeding incidence observed from the gut content analysis. Therefore, feeding incidences near 50 % indicate that it is possible for ctenophores to successfu l l y obtaining enough food to sustain metabolic needs during autumn and winter
65 CHAPTER FIVE SUMMARY C allianira antarctica was the dominant ctenophore in the Marguerite Bay reg ion with a widespread distribution during autumn and winter consist ing mostly of adult ctenophores The annual occurrence of this species, based on both literature accounts and this study, suggests that there is a stable, persistent population of C. antar ctica in the WAP region The mean abundance of C. antarctica during winter (0.45 ind. m 2 ) is significantly lower than ctenophore populations in temperate regions, but similar to the abundance of M. ovum found in the artic. Specific circulation features, such as the large clock wise gyre located over the north shelf where dense aggregations of ctenophores (>1 ind. m 2 ) were found may concentrate prey and predators within these areas, increasing chances of predation on zooplankton in an otherwise patchy e nvironment Ctenophores were mostly distributed in the upper 200 meters of the water column; however the depth of maximum abundance occurr ed within and just below the pycnocline where higher concentrations of prey may be found Day/Night tows indicat ing a sub maximum occurrence of C. antarctica in the upper 50 m at night, and ROV observations of large numbers C. antarctica directly under the sea ice with tentacles extended, suggests an increased predation impact on larval krill at night. C allianira anta rctica is a physically robust tentaculate ctenophore containing relatively high concentrations of carbon and nitrogen. C allianira antarctica s winter metabolic rates were within the range of rates reported for other ctenophore species from
66 the Antarctic a nd the Arctic, and lower than that for most ctenophores from temperate waters. Winter digestion rates of C. antarctica were slow compared with that of ctenophores from temperate and tropical habitats, and were highly dependent on prey type and number. Th e extended digestion times during winter may ultimately limit the amount of carbon ctenophores can process on a daily basis and, therefore, the amount of carbon available for growth or reproduction after metabolic requirements are satisfied. Despite the de crease in potential prey abundances between autumn and winter (Ashjian et al. in press), the fact that (1) average digestion times (e.g., 10.0 and 16.5 hours for prey items under 1.0 and 2.0 mg C, respectively) would allow multiple meals each day, and (2 ) about 50% of the collected ctenophores had food in their gastrovascular cavity suggest that C. antarctica may have been able to meet, and possibly exceed, the maintenance daily carbon requirement, even during winter. However length frequencies distribut ions from fall and winter suggest ctenophores may be experiencing degrowth in winter. Whether this decrease actually result ed from degrowth in ctenophores, or was the result of sampling two different populations is unclear. Diver observations, net collec tions and gut content analysis indicate that this species is an opportunistic predator that feeds on both copepods and krill during the day and night Lipid biomarker analysis and prey composition in the gut contents of ctenophores collected over autumn and winter suggest ctenophores do not utilize lipid reserves in times of low food availability, but instead may compensate for the seasonal decrease in prey abundance and increase in food patchiness by relying on under ice aggregations of larval and juveni le krill to sustain metabolic needs. Hen c e, d ense aggregations of C. antarctica under the ice could have significant affects on the recruitment of larval euphausiids
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Scolardi, Kerri Mannke.
Distribution, metabolism and trophic ecology of the Antarctic cydippid ctenophore, Callianira antarctica, west of the Antarctic Peninsula
h [electronic resource] /
by Kerri Mannke Scolardi.
[Tampa, Fla.] :
University of South Florida,
Thesis (M.S.)--University of South Florida, 2004.
Includes bibliographical references.
Text (Electronic thesis) in PDF format.
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Mode of access: World Wide Web.
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ABSTRACT: The distribution, abundance, chemical composition, metabolism, and feeding ecology of the tentaculate ctenophore, Callianira antarctica (Chun 1897), were investigated during austral winter 2001and autumn & winter 2002, in the vicinity of Marguerite Bay west of the Antarctic Peninsula. Callianira antarctica had a widespread distribution during autumn and winter, and variable abundance (0.02 to 2.6 ind. m-2) during winter 2001 associated with specific circulation features. Size frequency distributions for autumn and winter suggest that more than half of the C. antarctica population may have experienced 'degrowth' during winter due to low food availability. Callianira antarctica is a fairly robust ctenophore with geometric mean (geomean) carbon (C) and nitrogen (N) values of 8.41 and 1.83% dry weight (DW), respectively. Winter oxygen consumption and ammonium excretion rates ranged from 0.059 to 0.410 micro l O2 [mg DW]-1 h 1 and 0.60 to 31.1 ig-at N [g DW]-1 h-1, respectively, at 0oC. Daily minimum maintenance rations based on respiration experiments were 2.7% to 3.6% of the total body carbon (TBC) for small ctenophores, and 1.4% to 1.9% TBC for larger ctenophores. Calanoid copepods and larval and juvenile Antarctic krill were offered to ctenophores in incubation experiments. Digestion times were variable, lasting 8 to 20 h, and were independent of ctenophore size and dependent on number and type of prey. Gut content analysis from one autumn and two winter seasons indicated C. antarctica preyed on both copepods and krill in situ, with an increased dependence on larval krill during winter. Lipid biomarker analysis on C. antarctica and their potential prey confirmed these results. Divers observed aggregations of C. antarctica passively drifting with tentacles extended near dense concentrations of larval Euphausia superba during winter. These observations along with gut content and lipid biomarker analysis suggest that larval krill is an important prey item for C. antarctica during winter.
Adviser: Daly, Kendra L.
x Marine Science
t USF Electronic Theses and Dissertations.