VERTICAL DISTRIBUTION, ABUNDANCE AND FEEDING OF THE COPEPOD GENUS PLEUROMAMMA IN THE EASTERN GULF OF MEXICO by James L. Bennett A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in the Department of Marine Science in The University of South Florida December, 1986 Major Professor: Dr. Thomas L. Hopkins
Graduate Council University of South Florida Tampa, Florida CERTIFICATE OF APPROVAL MASTER'S THESIS This is to certify that the Master's Thesis of James L. Bennett with a major in Marine Science has been approved by the Examining Committee on November 17, 1986 as satisfactory for the Thesis requirement for the Master of Science degree. Thesis Committee: Major Professor: Thomas L. Hopkins Member: Norman J. Blake Member: Peter R. Betzer
ACKNOWLEDGMENTS I would like to thank my committee members for valuable comments and criticisms. To Dr. Tom Hopkins, my sincere gratitude for his persistence in guiding my efforts and for his friendship. ii
TABLE OF CONTENTS TABLES . . . . . . . . . . . . . . . . . . . . . iv LIST LIST OF OF FIGURES . . . . . . . . . . . . . . . . . . . . . v ABSTRACT ................................................ INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . Hydrography . . . . . . . . . . . . . . . . . . . . . METHODS . . . . . . . . . . . . . . . . . . . . . . . . . RESULTS . . . . . . . . . . . . . . . . . . . . . . . . Taxonomy . . . . . . . . . . . . . . . . . . . . . . Population Size . . . . . . . . . . . . . . . . . . . Vertical Distribution . . . . . . . . . . . . . . . . Feeding . . . . . . . . . . . . . . . . . . . . . . . DISCUSSION . . . . . . . . . . . . . . . . . . . . . . . Population Size and Structure Vertical Distribution and Migration vi 1 2 5 1 2 1 2 1 4 1 6 24 27 27 32 Feeding . . . . . . . . . . . . . . . . . . . . . . . 3 5 Pleuromamma as Prey .. 37 ECOLOGICAL SIGNIFICANCE LIST OF REFERENCES iii 4 2 44
Table 1 2 3 4 5 6 LIST OF TABLES Cruise dates and sampling data for R/V Columbus Iselin cruises to 27N 86W. Number of plankton tows at each depth horizon for various day and night periods (local time). Symbol (-) indicates no sample. Mean size measurements and formalin preserved dry weight of Pleuromamma individuals as determined from l east squares regressions (se e Methods). Population size summed over 0-1000 meters depth for day and night. Approximate depth in meters of the centers of population during the day Zd, the non-migrating copepodite population at night, Zn, and the migrating populations of adults and copepodites at n ight, Zm. Diet composition and diversity (see Methods) of Pleuromamma spp. Percentages represent incidence of occurrence, i.e., the portion of the twenty individuals o f each species examined having the indi c ated food items in their s tomachs. Mean percentage of stomach area filled with food (feeding index -see Methods) for adult females (twenty specimens) o f each spe c ies take n from the center of d istribution in various time p eriods. (-) indicates no data i v Page 5 7 1 3 1 5 25 26
LIST OF FIGURES Figure Page 1 (A) Sampling location ( 27N 86W) relative to the position of the loop current. (B) Representative vertical profiles of temperature and dissolved oxygen. 3 2 Size distribution of the four Pleuromamma species expressed as a percent total dry weight biomass and percent total numbers. 17 3 Vertical distribution of adults and copepodite stages of Pleuromammaabdominalis during the day and night. + represents 18 4 Vertical distribution of adults and copepodite stages of Pleuromammagracilis and Pleuromamma piseki during the day and night. + represents < 3. 21 5 Vertical distribution of adults and copepodite stages of Pleuromammaxiphias during the day and night. + represents 23 6 Day and night vertical distribution (percent total biomass) of Pleuromamma spp. > 1.5 mm total length compared to the vertical distribution of micronekton known to feed on Pleuromamma. Vertical distribution of micronekton is shown during their primary feeding periods. Micronekton data derived from referenced data from the eastern Gulf of Mexico (27N 86W). Group designations refer to the foraging depths designated in the figure. 39 v
VERTICAL DISTRIBUTION, ABUNDANCE AND FEEDING OF THE COPEPOD GENUS PLEUROMAMMA IN THE EASTERN GULF OF MEXICO by James L. Bennett An Abstract Of a thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in the Department of Marine Science in The University of South Florida Major Professor: Dr. Thomas L. Hopkins vi
The copepod genus Pleuromamma is an important forage resource in the epipelagic and mesopelagic zones of temperate to tropical latitudes. In the eastern Gulf of Mexico, representatives of this genus dominate the copepod assemblage both the day and night over a broad depth range. Species of this genus undergo strong diel migration and two species assemblages are identified during the night. The largest species, xiphias remains at or below 100 meters at night whereas the other three species abdominalis, gracilis, and piseki) move well into the upper 100 meters, some reaching the surface. Adults of P. gracilis and piseki co-occur both during the day and during the night. During the day the adults of all four species remain well below 250 meters with the depth of occurrence of the center of the adult population being directly related to the size of the adult of the species. Copepodites of each species demonstrate an ontogenetic migration pattern with earlier stages of development living at shallower depths during the day. For all species, only a portion of the copepodites of all species migrate above 200 meters during the night with the non-migrating portion of the population remaining at or below the daytime population centers. vii
The principal foraging periods for the adults of all species occur during the night with the prey consisting of a variety of phytoplankton, zooplankton and probable detrital material, all of which is characteristic of the diet of omnivorous copepods. The feeding index of each species was significantly different from the other species with the larger species having the higher feeding index as well as the greater diversity of diet. Abstract approved: viii Major Professor Professor: Department of Marine Science Date of Approval
INTRODUCTION The calanoid copepod genus Pleuromamma is an important representative of the oceanic plankton between latitudes 60N and 60S (Steuer, 1932; Brodskii, 1950; Fleminger, 1956; Owre and Foyo, 1967; Park, 1970; Hopkins, 1982). It is often abundant and is conspicuous in plankton catches because of a dark metasomal pigment spot. Members of this genus are strong diel vertical migrators and may be found in oceanic waters from the surface to 1000 meters (Steuer, 1932; Moore, 1949; Brodskii, 1956; Moore and O'Berry, 1957; Heinrikh, 1957; 1958; Kuenzler, 1965; Bowman, 1971; Roe, 1972b; 1984; Timonin, 1971; Hure and de Carlo, 1974; Deevey and Brooks, 1977; Hopkins, 1982). The larger species, which can exceed 5 mm in length, can cover 600 700 meters during a diel migration, some reaching the surface waters at night. The genus Pleuromamma is an important forage item for many species of midwater fishes and shrimps (Foxton and Roe, 1974; Merrett and Roe, 1974; Hopkins and Baird, 1977; 1981; Heffernan and Hopkins, 1981; Gorelova, 1981; Clarke, 1980, 1982; Kinzer, 1982; Roe and Badcock 1984) and there is evidence that members of this genus may be preferential food for mesopelagic zooplanktivorous fishes, ( e.g. Clarke, 1980; Baird and Hopkins, 1981; Scotto di Carlo, et al, 1982; Hopkins and Baird, 1985). Pleuromamma xiphias,
2 f. abdominalis, f. gracilis and P. piseki are the abundant representatives of the genus in the Gulf of Mexico (Fleminger, 1956; Park, 1970; Hopkins, 1982) and the following presents information on abundance, diel vertical distribution, diet, and feeding chronology of these species. Hydrography Samples were collected during the summer months at 27N and 86W in Loop Transition or "boundary" waters (Jones, 1973) adjacent to the eastern Gulf of Mexico Loop Current (Figure 1A). The Loop Current is generated when water of Caribbean origin, the subtropical undercurrent, pulses into the Gulf forming an anticyclonic intrusion which enters through the Yucatan Straits and exits through the straits of Florida. (Leipper, 1970; Nowlin, 1971; Maul, 1977; Molinari and Mayer, 1980). The Loop Current is identifiable by the depth of the 22C isotherm, which is located between 150 200 meters. The position of the boundary of the Loop Current in June 1975 and 1976 in the eastern Gulf is shown in Figure 1 A. Surface temperatures in "boundary waters" are between 28-30C in the summer and the mixed layer extends to 30-50 meters (Figure 1B). Temperatures at the base of the steepest gradient of the thermocline, at approximately 150 meters, are 15-18C, decreasing to 8-9C at 500 meters, then to 4-5C at 1000 meters. The eastern Gulf is well oxygenated with the minimum for the water column (-450
A GULF OF MEXICO JUNE '\975 8 100 200 E I .,._ Cl. w 0 300 400 500 TEMPERATURE 10 15 20 Figure 1 (A) Sampling location ( A -27N 86W) relative to the position of the loop current. (B) Representative vertical profiles of temperature and dissolved oxygen. w
meters) exceeding 2.7 ml 02/liter (Nowlin, 1971; Hopkins and Lancraft, 1984). 4 The water is oligotrophic with an estimated primary productivity of less than 50 g C/m2/yr (El-Sayed, 1972; Hopkins, unpublished data) and a zooplankton standing crop of 1.2 g DW/m 2 in the upper 1000 meters (Hopkins, 1982). Species diversity is high with 21 genera of zooplankton each constituting more than 1 percent of total zooplankton biomass in the upper 1000 meters (Hopkins, 1982).
5 METHODS Samples for this study were taken on three consecutive summer cruises of R/V Columbus Iselin during June 1975 and 1976 and late September 1977 (Table 1). Horizontal tows were made at 22 depth horizons at various times in the diel period. Only day and night tows are considered here in the vertical distribution analysis. The dawn and dusk tows were excluded since there were few tows at those times and also because the Pleuromamma spp. were vertically migrating during those times. Table 1 Cruise dates and sampling data for R/V Columbus Iselin cruises to 27N 86W. Primary Tow Mean Sampling Duration Sample Horizons Range No. Volume Cruise Dates (meters) (hrs) Tows ( m 3) C-I 6/75 0 200 1 0 -1 5 56 642 C-II 6/76 200 550 1 5 2.0 27 917 C-III 9/77 500 -1000 1 5 2.0 18 1986 Sampling was with collapsible plankton nets mounted in the mouth of a messenger-operated closing Tucker trawl as described in Hopkins, et al. (1973) and Hopkins and Baird (1975). The plankton nets were of 162 urn mesh and had a 1:5 mouth width to length ratio. The net mouth was square in
configuration and either 44 x 44 em or 66 x 66 em in dimensions. Towing speed was 1.5 -2.5 knots and tow duration was 45 minutes in the upper 50 meters and 60 to 120 minutes at deeper horizons (see Table 1). 6 Sampling depth was monitored with wire angle measurements for depths less than 50 meters and with a depth transducer and digital deck readout system when sampling below 50 meters. A time-depth recorder attached to the trawl provided a depth trace for each tow. Volumes filtered were estimated with mechanical dial-type flowmeters suspended in the mouth of the net (see Table 1). Only those samples for which the trawl successfully opened and closed and which had stable horizontal time/depth traces were analyzed (see Table 2). Samples were preserved in seawater-formalin (10% v:v) for subsequent analysis ashore. For counts, samples were split with a Metoda box (Metoda, 1953). One aliquot per sample was analyzed, the aliquot ranging from 1/64 to the entire sample depending on Pleuromamma abundance. Late stage and adult Pleuromamma in aliquots were identified to species. Only adults were identified to sex. Early stage copepodites were identified to species when possible. All individuals irrespective of stage of development were measured when 1 00 or less were present in an aliquot. The frequency distribution of metasomal length was analyzed with probability paper (Harding, 1949) this being used to
7 Table 2. Number of plankton tows at each depth horizon for various day and night periods (local time). Symbol (-) indicates no sample. Depth Day Night ( m) (0800-1500) (2000-0300) 0 4 5 5 1 1 1 0 3 3 1 5 2 4 30 1 3 50 5 4 75 3 1 00 3 6 150 1 3 200 2 2 250 1 300 2 3 350 2 2 400 3 2 450 2 1 500 2 2 550 3 2 600 2 2 700 2 1 800 2 1 900 2 3 1000 1 2 Total 45 56
8 determine the mean and size range for adult and identifiable copepodite stages. For biomass estimates, formalin preserved individuals were measured, rinsed briefly in freshwater, blotted dry, then placed in aluminum pans according to species and developmental stage, and put under vacuum desiccation. Weighing was after eight days of desiccation, with relative-ly constant dry weight being achieved after five days (see Lovegrove, 1966). Weighing was on a Mettler(R) balance to the nearest 0.1 mg or 0.01 mg depending on sample weight. A regression of dry weight (DW) on metasome length (ML) was calculated for each species, with the first order approxima-tion being adequate on the basis of high r2 values: P. xiphias log DW = -2.152 + (0.555)ML [r2 = 96.2] P. abdominalis log DW = -2.688 + (0.909)ML [r2 = 93.1] P. gracilis/piseki log DW = -2.859 + (1 .136)ML [r2 = 71.2] On the basis of Mullins and Evans's (1974) results, it was assumed that only minimal losses of organic material occurred during the period that Pleuromamma was stored in buffered formalin. The abundance of the various copepodite stages of each species was determined for every sample and means were calculated for all replicate samples within a designated time period. The means were integrated over the depth horizons sampled to yield estimates of the number of indivi-duals under 100 square meters of sea surface from the
9 surface down to 1000 meters depth. Vertical migration patterns were analyzed by determining the depth centers of populations during the day and night. The depth center was defined as that level below which 50 percent of the total population of a particular species or stage of development resided. Because not all individuals underwent migration, the nighttime depth center of the migrating portion of the population was defined as that level below which 50 percent of the population found between 0-200 meters resides. Species biomasses were estimated by determining mean weight of individuals for each size class using the size/weight regressions, then multiplying this weight by the number of individuals under 100 m2 of the sea surface. Vertical separation of the adults of each species was tested statistically by Whittacker's (1952) percent similarity index of association: n PS = 100 i=l ai -bi ) where PS is the similarity index and ai and bi are the fractions of the total catch of a and b species in the ith depth interval represented by the catch of species a and b. The index ranges from 0-100 and values greater than 60 were considered to indicate co-occurrence (Donaldson, 1975). Only females were used in the feeding study analysis because they were more numerous than males and because both sexes of Pleuromamma are reported to have similar feeding patterns (Hayward, 1980). For all four species, feeding
1 0 chronology was investigated by sorting twenty adult females from samples from the depth centers of day (0800-1500 hours) and night (2000-0300 hours) distribution. Estimation of a feeding index was a two stage procedure. Each specimen was cleared in lactic acid (Hume and Gooding, 1964; Hayward, 1980) and subjectively scored on the fraction of the stomach area filled with food when viewed at 500X magnification under a compound microscope. The gut was defined as that widened portion of the alimentary canal or mid-gut (Dakin, 1908) from the penultimate segment of the thorax to the beginning of the rostrum. The copepod was then dissected to verify the scoring by moving aside the developing eggs that may have interfered with the estimate. In the case of P. abdominalis, additional sets of twenty females were selected from both sunrise (0300-0800 hours) and sunset (1500-2000 hours) centers of distribution to describe the diel feeding cycle in greater detail. The feeding indices were compared through use of the non-parametric Mann-Whitney Q statistic (Sokol and Rohlf, 1969), this being a two-sample test based on measurement rankings. For diet composition analysis, gut contents of twenty females of each species with full stomachs were spread on a slide and mounted in a water base media (CMCP-AF Macmillan Scientific Co. Inc.) with acid fuschin stain. The slides were examined under an oil immersion using phase contrast, and r ecognizable items were tallied for each stomach. Species diet compositions were compared using a
modification of the information index (Travers, 1971), the equation being: where D = the diversity index with a range of 0 -3.33, N = Total incidence (=100%) of all catagories of food, and n = the incidence (%) of a single food type. 1 the incidence of each food type was calculated as a percent of the total number of incidences of all types of food recorded from a species sample of stomachs (see example in Hopkins, 1 985). 1 1
1 2 RESULTS Taxonomy Pleuromamma xiphias forma typica and gracilis forma minima, the dominant forms of these two species in the tropical Atlantic (Steuer, 1932), were the only forms of these species found in our collections. piseki was originally considered to be a form of P. gracilis but now is recognized as a separate species (Bowman, 1971). Both species were common in the eastern Gulf of Mexico and frequently occurred in the same sample. The edentata and typica forms (Steuer, 1932) of P. abdominalis were found in our collections, the former being represented by only a few specimens taken between 350 and 500 meters and at 50 meters. The abundant typica variant of both sexes of adult P. abdominalis was represented by large and small forms (see table 3). A large:small size ratio averaged 1.3:1, though variations in the degree of spination in the first antennal spines, a key characteristic in distinguishing different forms of P. abdominalis (Steuer, 1932), appeared to be differences of scale attributable to the differences in individual size, not to differences in kind. Identification of the copepodite stages III V of P. xiphias and P. abdominalis was based on the presence or
Table 3. Mean size measurements and formalin preserved dry weight of Pleuromamma individuals as determined from least squares regressions (see Methods). Species Stage of Development Pleuromamma xiphias adult female adult male copepodi te V copepodite IV copepodi te III Pleuromammaabdominalis adult female (small) adult female (large) adult male (small) adult male (large) copepodi te V copepodite IV copepodi te III Pleuromamma piseki adult female adult male Pleuromamma gracilis adult female adult male Pleuromamma gracilis/piseki copepodite V copepodite IV Total Length (mm) 4.58 4.81 3.39 2.4 7 1 71 2.81 3.1 8 2.85 3.24 2.32 1. 70 1 .3 6 1 .84 1. 76 1.81 1. 76 1 .39 0.82 Regression Meta somal Meta somal Dry Weight Length(mm) Width(mm) (mg) 3.28 1.06 0.465 3.44 1 1 8 0.570 2.43 0.80 o. 1 57 1. 77 0.53 0.068 1 .23 0.34 0.034 1.98 o. 78 0.1 3 6 2.23 0.81 0.21 8 2.01 0.86 0.1 38 2.27 0.93 0.237 1 .65 0.60 0.065 1 .2 3 0.45 0.027 1 .oo 0.32 0.01 7 1.2 9 0.50 0.040 1.17 0.43 0.030 1 .27 0.46 0.038 1 1 7 0.43 0.030 0.99 0.35 0.01 8 0.61 0.24 0.007 __. w
1 4 absence of the rostral prominence characteristic of P. xiphias. P. xiphias/abdominalis copepodite stages I -II and P. gracilis /piseki copepodite stages I -III were rarely encountered in our sample aliquots. Mean sizes of all adults and copepodites are shown in table 3. Pleuromamma guadrangulata has not been previously reported in the Gulf of Mexico but occasional late copepodites of that species were encountered in the present study at depths ranging from 75 to 300 meters. Population Size Nighttime estimates for populations of all species in the 0-1000 meter zone were consistently below those for the day except for E abdominalis adults (see Table 4). The differences between the day and night estimates for numbers in the upper 1000 meters, expressed as a percent of the mean was higher (71%) than for the biomass (42%). The best estimates of population size and structure were found in the day samples, with over 85 percent of the day residence depth zone of all species being sampled during a single cruise (CII). The highest abundance estimates were also found during this time. The total biomass of Pleuromamma species for the day (7569 mg/1 00m2 ) was very close to that found by Hopkins (1982) for this location, 7734 mg/100m2 based on a separate analysis of the same samples. Combining all stages of Pleuromamma species taken by the nets, the dominant size class both in terms of biomass and numbers was between 1-2 mm total length; less than 2 percent of the biomass and 1 5
Table 4. Population size summed over 0-1000 meters depth for day and night. Approximate depth in meters of the centers of population during the day, Zd, the non-migrating copepodite population at night, Zn, and the migrating populations of adults and copepodites at night, Zm. Species Stage of Development Pleuromamma xiphias adult females males copepodite V copepodite IV cope pod ite I I I Total Pleuromamma abdominalis adult females males copepodite V cope pod i te IV cope pod i te I I I Total Pleuromamma gracilis adult female male Pleuromamma piseki adult female male Pleuromamma gracilis/piseki copepodite V copepodite IV Total (with adults) Ple urom
percent of the numbers of Pleuromamma occurred in the <1mm fraction of our collections (see Figure 2). 1 6 Pleuromamma gracilis was the most numerous species and P. xiphias the least numerous. piseki and P. abdominalis were intermediate in abundance, with the former being slightly more numerous than the latter. The trend in Pleuromamma then, is for population size to be inversely proportional to species size. The age structure data (see Table 4), however, indicated that some later copepodite stages were more abundant than earlier stages (see Discussion). Of the total Pleuromamma spp. biomass captured during the day, approximately 37 percent was abdominalis, with P. xiphias and gracilis/piseki each contributing approximately 31 percent. Adults contributed approximately 57 percent of the total species biomass collecte d for both P. xiphias and abdominalis and contributed approximately 82 percent of the total species biomass for gracilis/piseki. Vertical Distribution Pleuromamma abdominalis By day adults of P. abdominalis were deeper than the immature stage s and the centers of distribution became increasingly shallow for progressively younger stages (see Figure 3 and Table 4). By night, ninety-six percent of the adult numbers of P. abdominalis and approximately thirty -
Figure 2 Size distribution Pleuromamma species expressed as a percent total dry weigh t biomass and percent total numbers. 70 r-;-;-1-e e I .: .. OeiOMASS : .. t::J NUMBERS ... - .. 1-. 1- r--- le ..... . ..... ..... 1- ... : r-. e e e I ... :.I : .. e I .. : e e . I ... .. . : .. fe. I .. le __.._. eo z 0 50 .,_ (/') 0 Cl. 40 0 (.) .,_ 30 z w (.) a: w Cl. 20 10 <1 1-1.9 2-2.9 3-3.9 >4 TOTAL LENGTH (mm) 1 7
Pleur omamma abdomina/is DENSITY # /100m3 ADULTS v IV Ill DAY NIGHT DAY N I GHT DAY NIGHT DAY NIGH T 48 38 24 12 20 40 80 80 110 80 40 20 12 24 311 4 8 10 110 40 20 12 24 311411 411 38 24 1 2 8 1 8 2 4 32 s 10 20 30 60 56 40 50 + 66 53 60 70 .115 E 80 :I: 90 .... a.. 100,..-:; UJ ;...--+ 0 200 + 300 ssc:::::j 400 500 + 600 + + + 700 + + eoo + &00 + 1000 + + Figure 3 Vertical distribution of adults and copepodite stages of Pleurornarnrna abdorninalis during the day and night. + represents 2 OJ
eight percent of each copepodite stage numbers were above 200 meters. 1 9 Adults in the upper 100 meters had a primary density maximum between 5 and 10 meters and a secondary density maximum between 50 and 75 meters. Copepodites v, IV and III had primary density maxima at 30 meters and copepodite stage V had a secondary peak in density between 5 to 10 meters. Depth centers for the migrating portion of the population were progressively shallower for younger stages except for copepodite stage III (Table 4). Eighty-six percent of the P. abdominalis biomass moving above 200 meters at night was constituted by the adults. Diel vertical shifts of the migrating population centers of P. abdominalis adults and copepodite stages V, IV and III were, respectively, 300, 270, 250 and 225 meters. Thus, the more mature stages appeared to migrate over greater distances. During the day, calculated adult female and male population centers were both between 350 and 400 meters with the female center being slightly shallower. At night however, the female center was 50 meters and center for the males was between 75 and 100 meters. At 50 meters, the nighttime female: male ratio was elevated to 5:1 which was much higher than the day ratio at 400 meters of 1.3:1. Pleuromamma gracilis and Pleuromamma piseki Because of similarities in size, vertical distribution, and the difficulty of taxonomically separating all but the
20 adult stages, gracilis and piseki were considered together. During the day, adults of both species had population centers at approximately 300 meters. Copepodite stages V and IV had population centers between 200 300 meters and between 150200 meters respectively (see Figure 4 and Table 4). During the night, an average of 83 percent (11 percent difference) of the adults of both species and 29 percent (zero percent difference) of their combined copepodites were found above 200 meters. The migrating adults of gracilis and P. piseki had nighttime population centers at 60 and 80 meters respectively. Above 200 meters, copepodite stage IV individuals had a population center that was deeper than either the adult or copepodite stage V population centers. Pleuromamma and piseki adults and copepodites V and IV had diel vertical shifts of population centers of approximately 220, 250, 200 and 40 meters, respectively. During the day, calculated adult female and male population centers for both species were approximately equal at 300 meters. At night, however, the calculated population centers for P. gracilis females was between 75 and 100 meters and the center for the males was between 100 and 150 meters. At night the female P. piseki population center was slightly shallower than that of the males with both being between 50 and 75 meters.
e P. rrac/1/s ADULTS DAY NOHT grac/1/s/piseki DENSITY# /100m3 P. plsdi ADUlTS DAY NGHT v DAY NGHT IV DAY NIGHT teo t:ro 11o 40 2o 4o eo eo 110 eo 4o 20 20 4o eo 110 eo eo 40 20 2o4o 110 eo 1110120110 40 20 4o eo eo 8 10 20 30 ----164 + + ++ + + + + + + + + + + + + Figure 4. Vertical distribution of adults and copepodite stages of Pleuromamma gracilis and Pleuromamma piseki during the day and night. + represents N
22 The day female:male ratio for gracilis at 300 meters is high (5.3:1 ). At the same depth, the female:male ratio for P. piseki is low (0.89:1). Those ratios change during the night with moderate ratios ranging from 1.3 -1.7:1 for P. gracilis and P. piseki respectively. Pleuromamma xiphias During the day, the adults of xiphias were the deepest dwelling of all the Pleuromamma species with a center of distribution lying between 450 and 500 meters (see Figure 5). Copepodite stages V, IV and III populations centers were at progressively shallower depths (see Table 4). The vertical distribution of the combined b iomass of adults and copepodites closely followed that of the adults. During the night both adults and copepodites migrated into the upper 200 meters (Figure 5). Approximately 80 percent of the adult population were found above 200 meters, whereas only 37, 41 and 8 percent of copepodite stages V, IV and III respectively, were found above 200 meters at night. Population centers above 200 meters at night showed an ontological depth progression with the youngest copepodite stage being shallowest. The vertical diel shifts in the migrating population centers of P. xiphias adults and copepodite stages V, IV, and III from day to night were approximately 345, 235, 200 and 195 meters, respectively. During the day, the calculated adult female population center was 450 meters while the center for the males was
-E I 1-a.. LU c s 10 20 30 40 50 80 70 80 90 ADULTS NIGHT DAY DAY 16 12 8 4 4 6 12 16 16 12 6 4 100.....--: /-' 200 300 400 500 800 700 800 800 1000 Pleuromamma xiphias DENSITY # /1OOm 3 v IV NIGHT DAY 4 6 12 16 32 24 16 8 Ill NIGHT DAY NIGHT 4 6 12 18 24 16 12 8 4 12 1. Figure 5. Vertical distribution of adults and copepodite stages of Pleuromamma xiphias during the day and night. + represents < 3. IV w
24 approximately 500 meters. At night, as in the other species, the calculated population centers for females was shallower being between 100 and 150 meters while the center for the males was 150 meters. The daytime female:male ratio for f. xiphias at 450 meters was high at 2.3:1 while at night that ratio was 1.3:1 at 100 meters. Feeding Results of the analysis of gut contents of the four Pleuromamma species showed few differences in the diet (see Table 5). Food items in most cases were fragments and were not subjected to quantitative analysis. Recognition of many items was not possible, even those items with some structural pattern. The most common food items in the stomach of all species were crustaceans, diatoms and radiolarians, with these also being the most easily recognizable food items. The crustaceans were primarily copepodite stages of copepods but also included fragments of amphipods, small ostracods and euphausiid larvae. Copepod prey were primarily calanoids with some harpacticoid and cyclopoid debris. In only two cases were whole copepods found in the gut, those being Oncaea and Labidocera copepodites in the stomach of f. xiphias. Diatom fragments found in stomachs were of the large centrate disc type and small whole pennate diatoms. All other items encountered were rare except for the goldengreen material so often noted by investigators (Lebour, 1922; Heinrikh, 1958; Harding, 1974; Heffernan and Hopkins,
25 Table 5. Diet composition and diversity (see Methods) of Pleuromamma spp. Percentages represent incidence of occurrence, i.e., the portion of the twenty individuals of each species examined having the indicated food items in their stomachs. Food Items (%) Ul Q) Q) Ul I'll .j...) X Q) tJ"' I'll Ul Q) .j...) c: "0 I'll Ul Ul I'll I'll c: c: Ul c: ...c: Q) 14 Q) H c: I'll Ul .j...) c: tJ"' Q) Q) I'll Q) r-i "0 I'll Q) I'll 11-1 14 >. Q) tJ"' 14 r-i c: Q) r-i .j...) 0 Ul I'll I'll c: tJ"' 14 11-1 c: I I'll r-i I'll E c: 0 tJ"' 0 r-i c: r-i Ul .j...) 0 11-1 0 r-i .j...) I () E Q) 14 14 Ul .j...) 0 r-i .j...) Q) Q) r-i I'll "0 Q) Q) ;::l I'll c: "0 c: I'll ;::l 14 > 14 r-i r-i I'll r-i ...c: r-i 0 0 I'll r-i u 0 0 p:; E-i u co U) t9 E 0 Species P xiJ2hias 75 50 0 40 40 0 5 5 1 0 100 2.54 P abdominal is 40 60 5 50 1 0 5 0 1 5 0 100 2. 41 P. gracilis 35 20 0 5 5 0 0 0 0 100 1 58 P. J2iseki 40 20 0 1 0 5 0 0 0 0 100 1 7 3
1981 ). As those authors noted, the material had the appearance of fecal pellets or detritus. The stomach fullness analysis, using the Mann-Whitney u statistic, indicated that the feeding index of all species was significantly higher (p < .05) during the night than during the day (Table 6). Maximum feeding occurred at night and virtually ceased during the day. Table 6. Mean percentage of stomach filled with food (feeding index -see Methods) for adult females (twenty specimens) of each species taken from the center of distribution in various time periods. (-) indicates no data. Diel Period 26 Species Sunrise Day Sunset Night Pleuromamma xiEhias 3.35 51 7 5 Pleuromamma abdominal is 7.35 1 65 3.85 26.60 Pleuromamma Eiseki 0. 1 0 20.30 Pleuromamma gracilis 0. 1 0 23.55 The data for female P. abdominalis adults showed the feeding index during the sunrise and sunset periods w ere signifi-cantly different from each other and from the day and night feeding indices (P < 10%). The larger species of Pleuromamma had the greater diversity of die t composition see Table 5).
27 DISCUSSION Population Size and Structure Using Hopkins' (1982) data, Pleuromamma species account for 47 percent of the copepod biomass from 200 500 meters during the day. During the night, they account for 30 percent of the copepod biomass from 30-200 meters and 14 percent of the total copepod biomass from 200 500 meters. The genus Pleuromamma, then, is an important fraction of the total copepod biomass; accounting for 10.4 percent in the upper 1000 meters (Hopkins, 1982). A number of investigators have commented on the significance and frequent dominance of the genus Pleuromamma at certain depths both in terms of numbers, as in the Atlantic off the Canary Islands (Roe, 1972a; 1972b) and the Sargasso Sea (Deevey and Brooks, 1977) and in terms of biomass as in the Bering Sea (Heinrikh, 1957). Rank order of species abundance is gracilis > P. piseki > P. abdominalis > xiphias. A similar order of species abundance was infered for the western Atlantic off Cape Hattaras (Bowman, 1971) where the same four species of Pleruomamma were found. In waters off the Canary Islands in the eastern Atlantic, where additional species of the genus were found, abundance relationships among the four species
remained basically the same except that f. piseki was slightly more abundant than f. gracilis (Roe, 1972b). 28 Rank order of biomass contribution was P. abdominalis > P. xiphias > f. gracilis > f. piseki. Because of its larger size the least numerous f. xiphias almost matched P. abdominalis in biomass contribution. The biomass contribution, of the species of Pleuromamma, then, is different than the numerical contribution of the species. Numerous studies have recorded differences in the day and night catches for a variety of plankters (Baker, 1970; Banse, 1964; Clutter and Anraku, 1968; Roe, 1972a). In the case of Pleuromamma in the eastern Atlantic off the Canary Islands, Roe (1972b) found them to be more abundant in night than day catches and cites avoidance (both tactile and visual) and patchiness as possible explanations. In the present study, day catches even of the larger species were often greater than night catches, a phenomenon difficult to relate to avoidance. There is a large difference in the numbers of adults compared to some of the copepodite stages, especially in the case of f. gracilis/piseki (see Table 4). From this it is evident that some of the copepodite stages were missed in sample analysis, were not present or were poorly sampled. Because of the dark pigment spot on all stages of copepodites of all Pleuromamma species, overlooking individuals in sample analysis would be minimal. Assuming the population is in a low to moderate growth phase typical of summer
29 populations of these species (Deevey, 1971), age distribu-tion, expressed in the form of a size-frequency plot of moderate decreasing (negative) slope should describe the age distribution that was actually present at the time of sampling (Krebs, 1972). Assuming the nets captured adults and copepodite v of P. xiphias and f. abdominalis with 100 percent efficiency, extension of the slope of the age pyramid into copepodites IV and III of those species indicates a capture efficiency for post-naupliar stages of these species of 70 and 64 percent respectively. Using the size-weight regressions (see Methods) these figures translate into biomass capture efficiency for f. xiphias and f. abdominalis of 90 and 87 percent respectively. Based on the average of the slopes for the other two species, capture efficiency for P. gracilis/piseki is 38 percent for numbers and 60 percent for biomass. These calculations then suggest a relationship between animal size and capture efficiency. Vannucci (1968) has discussed the mechanics of copepod escapement through the mesh of plankton nets. Although the metasomal width of the copepodites of f. gracilis/piseki is larger than the diagonal dimension (-0.23mm) of the meshes of the nets used in this study, there is, nevertheless, evidence (Table 4) that losses did occur as a result of escapement. Measurements of f xiphias and P. abdominalis indicate that losses may occur at approximately the same metasomal width (0.32 0.35 mm). Copepodite stages absent
30 in this study have metasomal widths which lie well below the theoretical size retention ability of the nets. For the larger (IV, V) copepodite stages that appear to be adequately sampled, the data suggest that the Pleuromamma species populations during the summer are either stable or decreasing in the eastern Gulf. The slopes of the sizefrequency plots do not suggest an exponential growth phase. As this type of environment is oligotrophic during the summer, with low nutrient input to promote rapid growth (McGowan, 1974; 1977), a stable or decreasing growth pattern is not unexpected. Data on the seasonal fluctuations of phytoplankton and zooplankton nauplii populations in the eastern central Gulf of Mexico (Hopkins, unpublished data), indicates that population maximums occur during the winter months (only January data available) and decrease to much lower levels during the months preceding and following a moderate increase during July. Similar seasonal information on Pleuromamma species is available for the Sargasso Sea (Deevey, 1971; Deevey and Brooks, 1977). Deevey (1966) has shown that f. gracilis and f. piseki individuals are largest (ML) during the spring, smallest during the winter and intermediate in size during the summer. Metasomal lengths of f. abdominalis and f. piseki in our collections correspond to the intermediate size of summer populations of these species in the Sargasso Sea (Deevey, 1964). The size (ML) of the f. xiphias indivi-
duals, however, more closely corresponds to the spring maximum size for that species in the Sargasso Sea (Deevey, 1964). It is not known if this species generally attains a larger size in the Gulf or if nutritional and reproductive cycles for this particular species have different seasonal patterns in the two areas. The adult female:male (F:M) sex ratios for all species from the day data (Table 4) are lower than those found in the eastern Atlantic (Roe, 1972a). F:M ratio for P. gracilis is much higher than that for f. piseki as was found by Bowman (1971) in the western Atlantic off Cape Hattaras. 31 Hayward's (1981) evidence suggests f. piseki reproductive behavior may be related to its shallow vertical distribution. F:M ratios in the secondary population center (5-10 meters) at night, for both f. abdominalis and f. piseki, are high (4.9 and 2.3 respectively), suggesting possible active reproductive behavior. The upward migration of males of P. gracilis forma maxima has been shown to lag behind that of the females in the waters off New Zealand. (Bradford, 1970). Such behavior might help explain the apparent differences in the sex ratios at the shallow depths. Roe (1984) found that the females of P. gracilis were generally shallower than the males throughout the diel cycle in the northeast Atlantic. That same general pattern is applicable to all four species in this study. There were differences in the day and night overall sex
32 ratios. Roe (1972b) found that such differences are not uncommon for this type of study and attributed the differences to the same factors effecting variation in the overall population estimates. Vertical Distribution and Migration All four Pleuromamma species undergo diel vertical migration. The larger species and older stages of development live deeper in the water column and traverse a greater distance during their vertical migration. Similar trends have been noted for adults of the genus Pleuromamrna in the Florida Current (Moore and O'Berry, 1957) and for the eastern Atlantic off the Canary Islands (Roe, 1972b). During the day P. xiphias is the deepest dwelling species followed by P. abdominalis then both gracilis and P. piseki. Day population centers in the present study were approximately the same as those reported by Moore and O'Berry (1957) yet with all being shallower than in the study by Ro e (1972b). Roe (1972b) reports a clear separation of adults of P gracilis and P piseki during the day. No such separation is evident in the present study. During the night P. abdominalis adults have a shallower population center than all other species but other studies (Moore and o'Berry, 1957; Roe, 1972b) show gracilis and piseki adults to be the shallowest dwelling at night. The study by Ro e (1972b) did report large numbers of P abdominalis adults above 5 0 meters though that data was excluded from their vertical distribution study.
33 An ontogenetic migration pattern for f. abdominalis and P. gracilis in the upper 200 meters of the Adriatic Sea has been described by Shmeleva and Zaika (1973) wherein the younger stages are at depth and occupy increasingly shallower waters as they develop. The present results, although limited to the larger copepodites in f. gracilis, show the opposite pattern. The vertical distribution of Pleuromamma stages during the day and night is positively related to size. Regr essions o f size of P. abdominalis adults and copepodites on the depth of their centers of distribution both day and night are significant (p < .05). The degree of significance being slightly higher for the day (r2 = 0.99) than the night data (r2 = 0.95). Patterns of ontogenetic migration similar to the present study are reported for P. robusta in the north Atlantic (Longhurst and Williams, 1979). Using Whittacker's (1952) index of association to compare the ver t ical distribution of adults at night, it is see n that the r e are two distinct assemblages consis t ing o f the deeper dwelling f. xiphias which doesn't migrate extensively into the uppe r 100 meters at n ight and the thre e remaining species which do move w e l l into the upper 100 meters. These two assemblages are not cleanly i sola ted wh e n the data is teste d with the more rigorous Kruskal-Walli s test. In contr a s t to our data r esults, Ro e (1972a) found larg e numbers o f f xiphias adults in the s urface w a ters o f the eastern Atlantic off the Canary Islands.
During the night, the adults of f. abdominalis, P. gracilis, f. piseki, migrating copepodite stages IV-V of P. abdominalis and migrating stage v of f. xiphias have an asymmetrical bimodal distribution with a primary peak between 30 and 75 meters and a secondary peak between 5 and 10 meters. Pearre (1979) has discussed this type of distribution and suggested that it may indicate two migratory patterns: 1 ) A small portion of those populations are migrating further than the rest. 2) All are reaching the primary peak depth but all or some are migrating up into the secondary peak level 34 in an asynchronous manner with short residence times in the shallow waters. The adequately sampled copepodite stages of all species have an asymmetrical, polymodal nighttime distribution with a remarkably consistent percentage (approximately 35%) moving above 200 meters. In an attempt to distinguish between the deep and shallow copepodite populations, eleven female copepodite stage V from the nighttime deep (350 m) population center and fourteen female copepodite stage V from the shallow (30 m) population center of f. abdominalis were prepared for histological examination using the methods of Barszcz and Yevich (1976). Primary and maturing ova were measured and the results were compared with the appropriate t-test for significant differences in the mean size of primary and maturing ova.
The results indicate that there are significantly (p <35 .01) larger and more maturing ova in copepodite stage v female P. abdominalis at 350 meters in comparison with those copepodite stage V females found at 30 meters at night. The two portions of the copepodites, then, have different physical characteristics and probably only a portion of the copepodite stage V female P. abdominalis are migrating into the epipelagic zone at night and the remainder are staying at depth. The significance of this in terms of reproductive behavior and strategy is not yet understood. It may be that the migrating copepodites require the additional energy resources that the non-migrating copepodites have already obtained. A corollary to the foregoing may be that the non-migrating copepodites are avoiding the energy expenditure of migrating into the surface waters when it is not absolutely necessary. Why the pattern changes for the adults is not clear. The fact that sex ratios change as a result of migratory changes in distribution is a strong indication that breeding occurs more readily as a result of vertical migration into the shallower waters. Active breeding is energy demanding and if breeding is occurring in the shallow waters, this is an added pressure to migrate not present for the copepodites. Feeding There were no significant differences in the diets of the adults of the Pleuromamma species, though only gross
differences were detectable by the techniques used. The principal diet components suggest an omnivorous diet as others (Heinrikh, 1958; Harding, 1974; Hayward, 1980; Hopkins, 1985) have found for this genus. Diet diversity appears to be positively related to species size, a pattern repeated for the feeding index. There is evidence in this study that the larger animal is probably capable of covering greater distances. This capability provides greater opportunity to find not only more food but more diverse food in a food poor environment. The chronology data show that all species are cyclic feeders, with night being the principal foraging period. Similar results were found for these same species in the North Pacific Central Gyre (Hayward 1980). The nighttime feeding indices (i.e. measure of gut fullness; see Methods) for the present study are i n the high end of Hayward's ranges but the values for each species relative to the others are similar. The nighttime feeding index for each species was significantly different from the others with that of E xiphias being the greatest followed by P. abdominalis, E piseki and E gracilis (see Table 6). Feeding studies o f this type must be qualified by the fact that the longer tow periods during the day allow more 36 time for the animals to evacuate their guts. More intensive short tows are needed to minimize any bias in the data arising from this problem. Studies by H ayward (1980), th1 s as a potential source of error as his however, m1n1m1ze
37 results, based on twenty minute tows, are similar to ours. Though diets appear similar, in the present case resource partitioning among these four congeners is potentially enhanced by diel spatial separation and differences in feeding indices. However f. piseki and P. gracilis co-occur, are of similar size and have similar diets. More information is needed on the ecology of these two species. Pleuromamma as Prey As previously noted, the copepod genus Pleuromamma is an important component in the diet of many species of oceanic micronekton. For many species of midwater fishes, the optimum size for prey species usually ranges from 2-4 mm total length (Gorelova, 1978, 1981; Baird and Hopkins, 1981; Hopkins and Baird, 1981). In this size range are the adults of P. xiphias and f. abdominalis as well as copepodite stages of IV-V and V of those species, respectively. Adults of P. gracilis and f. piseki lie only slightly below that optimum range in total length. Members of this genus are robust calanoid copepods, are moderately pigmented, have a prominent metasomal pigment spot and have luminescent glands that are capable of emitting relatively bright flashes (Clarke et al., 1962). All these characteristics serve to increase Pleuromamma species' prominence in the spectrum of pre y available to a visually oriented zooplanktivorous fish or shrimp as well as to maximize the predator's visual field with respect to
Pleuromamma species (Baird and Hopkins, 1981). 38 Members of the genus Pleuromamma undergo die! vertical migrations similar to many important species of midwater fishes. In the Gulf of Mexico, the primary layers of migrating fishes as located by acoustic sounding of the deep scattering layers are located below 400 meters during the day. At night, a portion of the deeper populations remain at depths of 300-500 meters while another portion moves into the shallow waters generally above 150 meters (Zahuranec, et al, 1970; Baird and Wilson, 1976). The coincidence of the vertical distribution of many migrating and non-migrating zooplanktovores at the time of their maximum foraging activity with the distribution of Pleuromamma spp. is illustrated in Figure 6. Many of these migrating species, notably the myctophid and gonostomatid fishes and sergestid shrimps, have maximum feeding times during the night in the upper 150 meters and feed heavily on Pleuromamma (Judkins and Fleminger, 1972; Merrett and Roe, 1974; Hopkins and Baird, 1977; Gorelova, 1978; Clarke, 1982; Kinzer, 1982; Roe and Babcock, 1984). One of the myctophid fishes, Lampanyctus alatus apparently selectively feeds on Pleuromamma spp. (Hopkins and Baird, 1985). This heavy reliance by migrating mesopelagic zooplanktovores on similarly migrating prey is the basis of a mesopelagic trophic complex of animals with fairly stable food and reproductive relationships (Gorelova, 1 97 8)
Figure 6. Day and night vertical distribution (percent total biomass) of Pleuromamma spp. 1.5 mm total length compared to the vertical distribution of micronekton known to feed on Pleuromamma. Vertical distribution of micronekton is shown during their primary feeding periods. Micronekton data is derived from referenced data from the eastern Gulf of Mexico (27N 86W). Group designations refer to the foraging depths designated in the figure. DAY FORAGERS Group #1 Gonostomatid fish Valencienellus tripunctulatus -day 200-400 m. Data from reference [1) Group #2 Sternoptychid fish Argyropelecus hemigymnus -day 300-400 m. Data from reference [1 ). Group #3 Gonostomatid fishes Gonostoma elongatum -day 500-550 m. and atlanticum -day 500-550 m. Data from reference [ 1 ] NIGHT FORAGERS Group #4 Myctophid fishes Benthosema suborbitale 80-130 m. Ceratoscopelus warmingii 80-130 m. Diaphus dumerilii-night 80-100 m. Lampanyctus alatus 80-130 m. Lepidophanes guentheri80-130 m. Lobianchia dofleini -night 80-130 m. Notolychnus valdiviae 80-130 m. Data from reference [1 ]. Group # 5 Penaeid shrimp Gennadas scutatus 150 m. Data from reference . Group #6 Sergestid shrimp Sergestes pectinatus50-150 m. corniculum 90-180 m. splendens 60-180 m. Data from reference . Group #7 Sergestid shrimp Sergestes sargassi 90-235 m. Data from reference . Group #8 Sergestid shrimp Sergestes !Obustus 1 50-300 m. Data from reference [3). Caridean shrimp Systellaspis debilus120-300 m. Data from reference . Group #9 Caridean shrimp Acanthephyra purpurea 300-350 m. Data from reference [4). Penaeid shrimp Gennadas valens 300 m. Data from reference [2). Group #10 Penaeid shrimps Gennada s bouvieri 350-550 m. G. capensis 350-550 m. Data from reference [2). REFERENCES 1 Hopkins and Baird, 1977 and Hopkins and Baird, unpubl ished data. 2 Heffernan and Hopkins, 1981. 3 Flock and Hopkins, unpublished data. 4 Gartner and Hopkins, in press.
,.... (j) c: w 1-w .._, J: 1a.. w 0 40 VERTICAL DISTRIBUTION P/euromamma app. PERCENT OF TOTAL BIOMASS 0 10 20 30 MICRONEKTON FORAGING ZONES (POPULATION maxima) DAY NIGHT 100 200 300 2 10 Pleuromamma spp. PERCENT OF TOTAL BIOMASS 30 20 10 0 300 400 500
41 Some deeper dwelling mesopelagic penaeid shrimp, notably the genus Gennadas, migrate from depths of 700 meters and feed heavily at night on Pleuromamma at depths of 300 meters (Heffernan and Hopkins, 1981). The Pleuromamma copepodite population that remains at those depths at night still forms a significant percentage (14 percent) of the available copepod biomass. Some Gonostomatids and Sternoptichids that do not vertically migrate feed during the day at depths ranging from 250-500 meters, the day residence depth range of the Pleuromamma population. The genus Pleuromamma forms a significant portion of the daily ration of many of those species (Merrett and Roe, 1974; Gorelova, 1981; Hopkins and Baird, 1981; Clarke, 1982; Roe and Badcock, 1984) and one species, Valenciennellus tripunctulatus (Sternoptichidae) has also been shown to selectively feed on Pleuromamma (Clarke, 1980; Baird and Hopkins, 1981 ). Pleuromamma species dominate the copepod biomass within their depth range of maximum abundance. That range often coincides with the depth of many mesopelagic zooplanktivorous micronekton species during their peak foraging periods. During at least one if not most of the stages of their postnaupliar ontogeny, members of the genus lie within the optimum prey size of many mesopelagic zooplanktivores. These characteristics help to explain why members of this genus appear as dominant prey for many mesopelagic zooplanktivorous micronekton.
ECOLOGICAL SIGNIFICANCE The stability of an open ocean food web increases when the diversity of the components that make up the food web 42 is high and when there are large numbers of predator/prey relationships within that food web. The population stability of a species is also directly related not only to the number of predators that feed on it but also to the number of species that serve as its food (Leigh, 1965). The fact that Pleuromamma spp. are linked as prey with many components of the micronekton while at the same time feeding on a variety of microplankton has ecological significance. By participating in such an extensive migration, Pleuromamma spp. are exposed to intensive predation during both the day and night. Under such high predation pressure, Pleuromamma spp. populations must have a high fecundity to be able to maintain such a dominant status in the copepod community. Nighttime migration into the food rich surface waters provides the energy needed to 11finance11 that fecundity. Nighttime migration, too, alters the sex ratios of the adults. This increases the opportunity for breeding. This balancing of energy and fecundity against predation pressure has developed as a strategy for success in part based on the generalist nature of the diet of Pleuromamma spp. Having a variety of microplankton that
43 serve as prey enhances the ability of Pleuromamma to feed in times when predation is high but food may be limited. This strategy increases the stability of the population. The complex relationship between Pleuromamma spp. and the many components of both the surface and midwater communities means that a stable Pleuromamma population, increases the overall stability of the food web structure. The micronekton species that prey on Pleuromamma are pan-oceanic in their distribution. The species of Pleuromamma studied here as well as other members of the genus occupy the same role from 25 30 northern to southern latitudes. The copepod genus Pleuromamma, then, illustrates a life strategy that balances the energy demands of a migratory strategy against intense predation pressure, and in so doing, contributes to the overall stability of what may be considered, by area, to be the single largest ecosystem on earth.
LIST OF REFERENCES Baird, .R.C., and .T.L Hopkins 1981, Trophodynamics of the f1sh.Valenc1ennellus tripunctulatus. II. Selectivity, graz1ng rates and resource utilization. Mar. Ecol. Prog. Ser., Vol. 5, pp. 11-1 9. -----44 Baird, R.C. and D.F. Wilson 1976, Sound Scattering and oceanic midwater fishes. In, Anderson, N., Zahuranec, (eds) Proceedings international symposium. Predictlon of sound scattering in the ocean. Plenum Press, New York, pp. 549-563. Baker, A. de c., 1970, The vertical distribution of euphausiids near Fuerteventura, Canary Islands. J. Mar. Biol. Assoc. Vol. 50, pp. 301-42. Banse,K. 1964, On the vertical distribution of zooplankton in the sea. Progress in Oceanography Vol. 2, pp. 53-125. Barszcz, C.A. and P. P. Yevich 1976, Preparation of copepods for histopathological examinations. Trans. Amer. Micros. Soc., Vol. 95, pp. 104-108. --Bowman, T. E. 1971, The distribution of calanoid copepods off the south-eastern United States between Cape Hatteras and southern Florida. Smithsonian Contributions to Zoology Vol. 96, 58pp. Bradford, J. M. 1970, Diurnal variation in vertical distribution of pelagic copepods of Kaikoura, New Zealand. N.Z. t!ar. Freshwater Resh. Vol. 4, pp. 337350. Brodskii, K.A. 1950, Calanoida of the far Eastern Seas and Polar Basin. USSR Academy of Sciences of the Union of Soviets Socialists Republic. Vol. 35, 440pp. Brodskii, K.A. 1956, On the vertical distribution of copepods in the north-western Pacific Ocean. Special Scientific Report Fisheries No. 192, pp. 1-5. Clarke, G.L. 1962, Comparative studies of lumenescence in copepods and other pelagic animals. J. Mar. Biol. Assoc. U.K. Vol. 42, pp. 541-564. Clarke, T. A. 1980, Diets of fourteen spec.i.es of migrating mesopelagic fishes in Hawa11an waters. F1sh. Bull., 74, pp. 619-640. Clarke T. A. 1982, Feeding habits of stomiatoid fishes from Hawaiian waters. Fish. Bull. Vol. 80, pp. 287304.
Clutter, R.I. and M. Anraku 1968, of samplers. In, Monographs on oceanographic methodology. 2. Zooplankton Sampling. The Unesco Press. Paris. pp. 57-76. Dakin, William J. 1908, Notes on the alimentary canal and food of the copepod. Int'l Revue der Gesamten Hydrobiologie. Vol. 1, pp. 772-78:;::--Deevey, G.B. 1964, Annual variations in length of copepods in the Sargasso Sea off Bermuda. ;z_. t!ar. Biol. Assoc. U.K. Vol. 44, pp. 589-600. 45 Deevey, G.B. 1966, Seasonal variations in length of copepods in south Pacific New Zealand waters. J. A st M _u_. Freshwater Resh. Vol. 17, pp. Deevey, G.B. 1971, The annual cycle in quantity and composition of the zooplankton of the Sargasso Sea off Bermuda I. The upper 500 m. Limnol. Oceanogr. Vol. 16, pp. 219-240. Deevey, G. B. and A. L. Brooks 1 977, Copepods of the Sargasso Sea off Bermuda : species composition and vertical and seasonal distribution between the surface and 2000 meters. Bull. t!ar. Sci. Vol. 27, pp. 256-291. Donaldson, H.A. 1975, Vertical distribution and feeding of sergestid shrimps (Decapoda: Natantia) collected near Bermuda. Mar. Biol. Vol. 31, pp. 37-50. El-Sayed, S.Z. 1972, Primary productivity and standing crop of phytoplankton. In, Chemistry, primary productivity, and benthic marine algae of the Gulf of Mexico. Serial Atlas of the Marine Environment. Amer. Geograph. Soc. Folio 22. Fleminger, A. 1956, the epopelagic Gulf of Mexico. pp. Taxonomic and distributional studies on calanoid copepods (Crustacea) of the Ph. D. Dissertation, Harvard Univ. 317 Fox ton, p. and H.S .F. Roe 1 9 7 4, Observations on the nocturnal feeding of some mesopelagic decapod crustaceans. !iar. Bio. 28: 37-49. Gorelova, T.A. 1978, The feeding of lanternfishes, Ceratoscopelus warmingii and Bolinichthys of the family myctophidae in the western equator1al part of the Pacific ocean. J. Ichthyol. Vol. 18, pp. 673-683. Gorelova, T.A. 1 981, Notes of feeding and gonad condi t.ion in three species of the genus Gonostoma (Gonostomat1dae). J. Ichthyol. Vol. 25, pp. 82-92.
46 Harding, 1949, The use of probability paper for the analysis of polymodal frequency distributlons. J. !iar. Biol. Assoc. U.K. Vol. 28, pp. 141-153. Harding, G.C.H. 1974, The food of deep-sea copepods. J. Biol. Assoc. U.K. Vol. 54, pp. 141-155. Hayward, T.L. 1980, Spatial and temporal patterns of feeding of oceanic copepods from the north Pacific central gyre. !1ar. _!3io1_. Vol. 58, pp. 295-309. Hayward, T.L. 1981, Mating and the depth distribution of an oceanic copepod. Limnol. Oceanogr. Vol. 26, pp. 274-377. Heffernan, J. J. and T. L. Hopkins, 1981, Vertical distribution and feeding of the shrimp genera Gennadas and Bentheogennema (Decapoda: Penaeidea) in the eastern Gulf of Mexico. J. Crust. Bio. Vol. 1, pp. 461-472. Heinrikh, A. K 1957, Vertical plankton distribution in the area southeast of Bonskii Island. Doklady Akademii nauk SSSR. Vol. 117, pp. 1007-1010. Heinrikh, A.K. 1958, ON the nutrition of marine copepods in the tropical region. Doklady Alademii nauk SSSR. Vol. 119, pp. 1028-1031. Hopkins, T.L. 1982, The vertical distribution of zooplankton in the eastern Gulf of Mexico. Deep-Sea Res. Vol. 29, pp. 1069-1083. Hopkins, T. L. 1985, Food web of an Antarctic midwater ecosystem. Mar. Biol. Vol. 89, pp. 197-212. Hopkins, T.L. and R.C. Baird 1975, Net feeding in mesopelagic fishes. Fish. Bull. U. S. Vol. 73, pp. 908-914. Hopkins, T.L. and R.C. Baird 1977, Aspects of the feeding ecology of oceanic mid-water fishes. In, Oceanic Sound Scattering Prediction -Mar. Sci. Vol. 2, edited by N. R. Anderson and B.J. Zahuranec, Off. Naval. Res!:.. pp. 325-360. Hopkins, T.L. and R.C. Baird Trophodynamics .of the fish Valenciennellus trlpunctulatus. I. Vertlcal distribution, diet and feeding chronology. Mar. Ecol. Prog. Sef.. Vol. 4, pp. 1-10.
Hopkins, T.L. and R.C. Baird 1985. Aspects of the trophic of the mesopelagic fish Lampanyctus alatus Myctophidae) in the eastern Gulf of Mexico. B1ol. Oceanog. Vol. 3, pp. 285-313. HoP k i n s T L. R. C. B a i r d and D. t-1. M i 11 ike n 1 9 7 3 A messenger-operated closing trawl. Limnol. Oceanogr. Vol. 18, pp. 488-490. 47 Hopkins, T.L. and T.M. Lancraft 1984, The composition and standing stock of mesopelagic micronekton at 27N 86W in the eastern Gulf of Mexico. Contrib. Mar. Sci. Vol. 27' pp. 143-158. ----Humes, A.G. and R.U. Gooding 1964, A method for studying the external anatomy of copepods. Crustaceana. Vol. 6, pp. 238-240. Hure, J. and B. S. de Carlo 1974, New patterns of diurnal vertical migration of some deep-water copepods in the Tyrrhenian and Adriatic Seas. Mar. Bio. Vol. 28, pp. 1 7 9-1 8 4 ----Jones, J.I. 1973, Physical oceanography of the northeast Gulf of Mexico and Florida Continental shelf area. In, A summary of knowledge of the eastern Gulf of Mexico. (Coordinated by the State University System of Florida Institute of Oceanography). Section IIB p. 1-11. Judkins, D.C. and A. Fleminger 1972, Comparison of foregut contents of Sergestes similis obtained from net collections and albacore stomachs. Fish. Bull. U.S. Vol. 70, pp. 217-223. Kinzer, J. 1982, The food of four myctophid fish species off northwest Africa. Reun. Cons. int. Explor 180, pp. 385-390. Krebs, c.J. 1972, Ecology -The experimental analysis of distribution and abundance. Harper and Row, New York. 6 9 4 pp. Kuenzler, E. J. 1965, Zooplankton isotope turnover during operation swordf1sh. Atom1c EneLgy Commission Report AT(30-1) 3145-1 WHOI Ref. Vol. 65, pp. 1-57. Lebour, M. 1922, The food of plankton orgainsms. J. Mar. Biol. Assoc. U.K. Vol. 12, pp. 644-667. Leigh, E.G. 1965, on the the productivity, biomass, diversity, and stab1l1ty of a community. Zoology Vol. 53, 777-783.
48 Leipper, D.F. 1970, A sequence of current patterns in the Gulf of Geophys. Res. Vol. 75, pp. 637-657. Longhurst, .A. and R . Williams 1979, Materials for plankton Vert1cal distribution of Atlantic zooplankton 1n summer. Plank. ReE_. Vol. 1, pp. 1-28. Lovegrove, T. 1966, The determination of the dry weight of plankton and the effects of various factors on the values obtained. In, Some contemporary studies in marine science. edited by J. Barnes. George Allen and Unwin Ltd., London. Maul, G.A. 1977, The annual cycle of the Gulf Loop Current. Part I. Observations during a one year time series. J. Mar. Res. Vol 35, pp, 29-47. McGowan, J.A. 1974, The nature of oceanic ecosystems. In, The biology of the oceanic Pacific. edited by C.B. Miller (ed) Oregon State University Press. Corvallis, Oregon. pp. 9-2 8. McGowan, J.A. 1977, What regulates pelagic community structure in the Pacific? In, Ocean sound scattering prediction. edited by N.R. Andersen and B.J. Zahuranec. Plenum Press, New York. Merrett, H.R. and H.S.J. Roe 1974, Patterns and selectivity in the feeding of certain mesopelagic fishes. Mar. Bio. Vol. 28, pp. 115-126. Molinari, R.L. and D. Mayer 1980, Physical oceanographic conditions at potential OTEC site in the Gulf of Mexico; 27N; 85.5\V. NOAA Tech. Memorandum ERL AOML. No. 42, 99pp. Moore, H.B. 1949, The zooplankton of the upper waters of the Bermuda Area of the North Atlantic. Bull. Bingham Oceanogr. Coll. Vol.12, pp. 1-97. Moore, H. B. and D.L. 0' Berry 1 9 57, Plank ton the F. lor current IV. Factors influenc1ng the vert1cal d1str1bution of some common copepods. Bull. Mar. Sci. Gulf Carib. VoL 7, pp. 297-315. Motoda, s. 1953, New Plankton Samplers. Bull. Fac. Fish., Hokkaido Univ. Vol. 3, pp. 181-186. Hullin M.M. and P.t-1. Evans 1 974, The use of a deep tank in plankton ecology. 2. Efficiency of a planktonic food chain Limnol. Oceanogr. Vol.19, pp. 902 -911.
49 Nowlin, W.D. 1971, Water masses and general circulation of the Gulf of Mexico. Oceanography International. Vol. 6, pp. 28-33. Owre, H.B. and Maria Foyo 1967, Copepods of the Florida Current. Fauna Caribaea, Vol. 1, 137pp. Park, T. S. 1970, Calanoid copepods from the Caribbean Sea and Gulf of Mexico 2. New species and new records from plankton samples. Bull. Mar. Sci. Vol. 20, pp. 472-546. ------Pearre Jr., S. 1979, Problems of detection and interpretation of vertical migration. J. Plank. Res. Vol. 1, pp. 29-44. Roe, H.S.J. 1972a, The vertical distribution and diurnal migrations of calanoid copepods collected on the SOND Cruise, 1965. I. The total population and general discussion.;[_. !:!ar. Biol Assoc Vol. 52, pp. 277-314. Roe, H.S.J. 1972b, The vertical distribution and diurnal migrations of calanoid copepods collected on the SOND Cruise, 1965. III. Systematic account: Families Euchaetidae up to and including the Metridiidae. J. !i_ar. Bio. Assoc Vol. 52, pp. 525-552. Roe, H.S.J. 1984, The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 4. The copepods. Prog. Oceanog. Vol. 13, pp. 353-388. Roe, H.S.J. and J.Badcock 1984, The diel migrations and distributions within a mesopelagic community in the north east Atlantic. 5. Vertical migrations and feeding of fish. Prog. Oceanog. Vol. 13, pp. 389-424. Scotto di Carlo, B., G. Costanzo, E. Fresi, L. Guglielmo and A. Ianora 1982, Feeding ecology and straining mechanisms in two lanternfishes, Hygophum benoiti and Myctophum punctatum. Mar. Mar. Ecol. Prog. Ser. Vol. 9, pp. 13-24. Shmeleva, A.A. and V. Y. Zaika 1973, Vertical distribution of copepodid stages of copepods in the Adriatic Sea. Oceanology. Vol. 13, pp. 722-725. Sokol, R.R. and F.J. Rohlf !he principles and practices of stat1st1cs 1n b1?log1cal research. w.H. Freeman & Company, San Franc1sco. 776 pp. Steuer, A. 1932, Copepode (6.):. Pleur?mamma Giesbr. 1898 der Deutschen Tiefsee-Exped1t1on. W1ss. Ergebn. dt. Tiefsee-Exped. "Valdivia", Vol. 24, pp. 1-119.
50 Timonin, A.G. 1971, The structure of plankton communities of the Indian Ocean. Mar. Bio. Vol. 9, pp. 281-289. Travers, M. 1971, Diversite du microplankton du Golfe de Marseille in 1964. !:!ar. Biol. Vol. 8, pp. 308 -343. Vannucci, M. 1968, Loss of organisms through the meshes. In, Ivlonographs on oceanographic methodology Zooplankton Sampling. The Unesco Press. Paris, France. pp. 77-86. Whittacker, R.H. 1952, A study of summer foliage insect communities in the great smoky mountains. Ecological Monogr. Vol. 22, pp. 1-44. Z a h u ran e c B J \'l L. Pugh and H. B. F a r q u h a r. 1 9 7 0 Biological sound scattering studies. Pt. I. Initial investigations in the Gulf of M exico and w e s tern north Atlantic. Tech. Rept. (TR-224), Naval Oceanographic Office. Washington, D.C., 35 pp.