Non-calanoid at the Bermuda Atlantic Time-Series Study (BATS) Station: Paper Number: OS35N-13 Community Structure and Ecology, 1995-1999 Hussain A. Al-Mutairi, Joseph J. Torres College of Marine Science, University of South Florida, 140 7th Avenue South, St. Petersburg, Florida 33701 Abstract was sampled on a monthly basis at the Bermuda Atlantic The cyclopoid was most abundant with an overall average had their highest numbers in the spring and summer with winter were much less pronounced than seasonal signals. Representatives of the Time-series Study (BATS) site from January 1995 to December 1999. of 4,769 individuals m-2. Following Oithona spp. in abundance were the being the season of lowest abundance. The one Poecilostomatoid group to Mormonilloida and were also frequently encountered, Samples were collected using a 1 m2, 200 μm mesh net towed obliquely Poecilostomatoid genera , Farranula and Corycaeus with 4449, counter this trend was the genus Lubbokia. L. squillimana, which made although in much lower numbers. Future work includes comparison of through the euphotic zone to a mean depth of 200m. One day and one 1712 and 1291 m-2, respectively. Harpacticoids were also up nearly 100% of this genus, was almost 3 times more abundant in results of this study to those of previous investigations conducted at night tow from each cruise was examined microscopically to determine common but about an order of magnitude less abundant at 114 m-2 and summer and fall than spring and winter. The harpacticoids on the other Hydrostation “S” in the same region. In addition to the community the community structure of the non-calanoid copepods. A total of 118 were dominated by Macrosetella gracilis. The most common hand were nearly 3 times more numerous in the fall and winter than in structure, the ecological roles in terms of C and N cycling of the Miraciid tows were examined and most copepods were identified to the level Poecilostomatoid species was Oncaea media with females alone accounting spring and summer. Generic seasonal trends were not necessarily harpacticoids and the Poecilostomatoid copepods of the genus Oncaea and with Oithona counted as a genus. The dominant orders in terms of overall for nearly half of all Oncaea copepods enumerated. Pronounced seasonal followed by each species. For example, Corycaeus speciosus was most family at BATS will be evaluated. abundance were the and . signals were noted. In general the genera Oithona, Oncaea, abundant in fall and Farranula gracilis had peak populations in fall. Corycaeus, Farranula, and Interannual trends, although present,

Introduction Results and Discussion Examples of non-calanoid copepods Seasonal Structure

The Bermuda Atlantic Time-series Study (BATS) in the Sargasso Sea (31º 50’ N, General Community Structure Copilia mirabilis male Copilia mirabilis female Pronounced seasonal signals in abundance were observed for the BATS non- 64º 10’W) was formed in 1988 as part of the US Joint Global Ocean Flux Study calanoid copepods in all years examined. Overall abundance of non-calanoid (JGOFS) program with the intent to better understand ocean biogeochemistry copepods was highest in spring followed by summer. Winter had the lowest Overall, the non-calanoid copepod community was dominated numerically by the numbers followed by fall. Oithona spp. had their highest abundance in spring and on seasonal as well as decadal time scales and in particular the role of the genera Oithona spp. and Oncaea spp. and they were nearly equal in abundance. world’s oceans in the carbon cycle (Steinberg et al. 2001). lowest in winter. Oncaea spp. were twice as abundant in spring and summer Roughly, they contributed approximately 60-80% of total non-calanoid copepod compared to fall and winter. Farranula spp. taken as a group masked the true numbers (range = 35,613 to 896 ind m-2). The next most important groups were the seasonal patterns made up by the 2 species F. gracilis and F, rostrata. Farranula An important driver of oceanic biogeochemical cycling is the biota. In fact, the genera Farranula and Corycaeus. Farranula spp. was generally twice as abundant as maintenance of the geochemical disequilibrium of carbon on earth is the result gracilis was nearly 10 times more numerous in summer and fall compared to Corycaeus spp. Together they comprised approximately 20-25% of overall non- winter and spring whereas F. rostrata was most abundant in spring. As a group of a myriad of comparatively small biological export processes in the ocean calanoid copepod abundance. The remaining groups, including the harpacticoids, Distioculus minor male Macrosetella gracilis female Corycaeus spp. had similar abundance in spring, summer and fall but were 3 times known collectively as the . Sapphirina spp., Copilia spp and Lubbockia spp. all contributed less than 5% of less numerous in winter. Most Corycaeus species had their highest abundance in total abundance. spring, however, there were some exceptions. Corycaeus speciosus was most Zooplankton (>200µm) contribute to the biological pump by producing abundant in fall and C. latus had its highest numbers in summer and fall. compact fast-sinking fecal pellets that contribute to gravitational fluxes Non-calanoid Families and Species identified at BATS (Paffenhofer and Knowles 1979; Small et al. 1983) and they augment recycling Sapphirina spp. and Copilia spp. had their highest abundance in spring with more by excreting nitrogen and other nutrients in the photic zone (Legendre and than double the numbers found in the other seasons. Whereas, Lubbockia spp. Rivkin 2002; Zhang et al. 1995). Lastly, zooplankton can actively transport (nearly 100% made up of L. squillimana) had its peak abundance in summer and Macrosetella gracilis Oculosetella gracilis Maracia efferata Distioculus minor elements out of the upper layers of the water column by excreting material at fall. Finally, the harpacticois were more numerous in winter and fall than spring depth (typically 300-600m) that was consumed in the sunlit regions of the ocean female Corycaeus speciosus male and summer. Theses results were in line with what Deevey (1971) found after (Longhurst et al. 1989; Steinberg et al. 2000 and Al-Mutairi and Landry 2001). analyzing one year of zooplankton samples taken at Hydrostation “S” near the Microsetella rosea Microsetella norvegica BATS station. Copepods are usually the most important component of the zooplankton generally comprising >70% of the total (Omori and Ikeda, 1984). They are therefore the dominant players in the passive and active transport of elements in the ocean. Most ecological and biological studies of copepods have focused on Clytemnestra scutellata Areas for Further Study the calanoids and much of what we know about pelagic copepod biology and •Examine the role of Miraciid harpacticoids in elemental alterations of Trichodesmium ecology is skewed towards them. However, the paucity of studies of the non- Farranula gracilis female spp. at the BATS site over a 3-year period. The goal would be to quantify the amount calanoid copepods (orders Cyclopoida, , Poecilostomatoida, Sapphirina metallina Sapphirina intestinata Sapphirina spp. Copilia mirabilis of nitrogen transferred from Trichodesmium spp. N2 fixation to the rest of the Siphonostomatoida and Mormonilloida) is not in keeping with their importance Copilia quadrata Copilia vitrea Vettoria granulosa Corissa parva autotrophic community as well as the role played by harpacticoids (e.g Macrosetella in the marine pelagic system. In fact, it just may be that the order Cyclopoida gracilis) in making Trichodesmium spp. organic carbon available to higher trophic represented by the family Oithonidae and the order Poecilostomatoida which levels contains the family Oncaeidae are the most numerous metazoans on earth (Bottgerschnack 1996; Gallienne and Robins 2001 and Hopcroft et al. 2001). Lubbokia squillimana Lubbokia aculeata Oncaea media Oncaea mediterranea Oncaea venusta Oncaea conifera Oncaea minuta Oncaea dentipes Oncaea venusta mating pair •Study the relationship between Poecilostomatoid copepod abundance (especially Pacos punctatum members of the genus Oncea) and larvacean abundance over a 5-year period as well as In addition to their numerical importance, certain groups of non- calanoid examine the role of Poecilostomatoid copepods in particulate matter degradation and 1995 BATS non-calanoid copepod abundance copepods can have ecological impacts that set them apart from most other Corycaeidae transformation. planktonic . Among these groups is the Poecilostomatoid genus 40000 35000 Oncea. Several studies have shown strong associations between Oncea spp. and Corycaeus speciosus Corycaeus clausi Corycaeus typicus Corycaeus limbatus •Analyze sediment trap Poecilostomatoida“swimmer” community structure at BATS 30000 Corycaeus flaccus Corycaeus latus Corycaeus lautus Corycaeus giesbrechtii Other non-calanoids discarded larvacean houses (e.g. as Alldredge 1972; Ohtsuka et al. 1993 and Total Copilia 25000 Corycaeus furcifer Corycaeus minimus Farranula gracilis Farranula rostrata Total Sapphirina Green and Dagg 1996). Total Harpacticoids •Estimate the capture efficiency of the 200μm mesh net of non-calanoid copepods by 20000 Total Lubbockia Total Corycaeus Total Farranula comparing samples collected by it and a 35μm mesh net at the BATS site. 15000 Oithonidae Total Oncaea

Number of individuals individuals of Number m2 Total Oithona Oncea species were found to preferentially feed on food collecting filters of 10000 discarded larvacean houses. This demonstrated the existence of a direct link Oithona spp. 5000 1996 BATS non-calanoid copepod abundance between nanoplankton (<20µm) that were concentrated by the filtering actions 0 30000

Rataniidae D 6th Nov

of the larvacean prior to abandonment and relatively large metazoans such as 11th N Jul 11th D Jul Apr 10th N Jan 11th N 11th Jan D 11th Jan Apr 11th D Apr 26th N Apr 27th D D 12th Jun N 12th Jun Oct 10th D 10th Oct Oct 10th N 10th Oct Mar 16th N 16th Mar Feb 14th N 14th Feb D 16th Mar Feb 14th D 14th Feb Dec 15th N 15th Dec D 16th Dec Sep 12th D 12th Sep N 12th Sep May 10th N 10th May D 11th May copepods that could not filter such small particles from the water column Aug 22nd D 25000 Other non-calanoids Ratania flava 20000 themselves. Another potentially important ecological role of non-calanoid Total Copilia Total Sapphirina Total Harpacticoids References copepods lies with the harpacticoid family Miraciidae that includes the species 15000 Total Lubbockia Total Corycaeus Pontoeciellidae Total Farranula Macrosetella gracilis. This family of copepods are well known associates of the Total Oncaea Alldredge A (1972) Abandoned Larvacean Houses - Unique Food Source in Pelagic Environment. Science 177:885-887 10000

Number of individuals individuals of Number m2 Total Oithona cyanobacterium Trichodesmium spp. Miraciid copepods, and Macrosetella Pontoeciella abyssicola Al-Mutairi H, Landry MR (2001) Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton. Deep Sea 5000 Research Part II: Topical Studies in Oceanography 48:2083-2103 gracilis in particular, have been shown to use Trichodesmium spp. colonies as a 1997 BATS non-calanoid copepod abundance

0 physical substrate as well as a source of food. In fact , as Bjonberg (1965) Mormonillidae 30000 N BottgerSchnack R (1996) Vertical structure of small metazoan , especially non-calanoid copepods .1. Deep Arabian Sea. h th N b 14th Nb 27th N p 2nd N e e Jul 8t Jul 10thAug D 5thAug D 5th Ne Oct 8 Nov 5th NovD 5th N demonstrated, Miraciid nauplii and copepodites were dependent on Jan 30thF N F Mar 15thMar N 27thMar N 28thApr D 22ndApr N 23rdMay D 7thJun N 10thJun D 10th N S Dec 11thDec N 14th D Journal of Plankton Research 18:1073-1101 25000 Trichodesmium spp. for survival. Mormonilla minor Deevey GB (1971) Annual Cycle in Quantity and Composition of Zooplankton of Sargasso Sea Off Bermuda .1. Upper 500 M. Other non-calanoids 20000 Total Copilia Limnology and Oceanography 16:219-240 Total Sapphirina Total Harpacticoids 15000 Total Lubbockia Studies by Roman (1978), O'Neil et al. (1996) and O’Niel (1998) have confirmed Total Corycaeus Gallienne CP, Robins DB (2001) Is Oithona the most important copepod in the world's oceans? Journal of Plankton Research 23:1421- Total Farranula Total Oncaea 1432 10000 on the ability of M. gracilis as well as other species of Miraciid harpacticoids to Total Oithona ingest Trichodesmium spp. and assimilate its carbon and nitrogen. These results meter square per individuals of Number Green EP, MJ Dagg. (1997) Mesozooplankton associations with medium to large marine snow aggregates in the northern Gulf of 5000 point to their importance as a direct link between cyanobacterial production 1998 BATS non-calanoid copepod abundance Mexico. Journal of Plankton Research 19: 435-447. 0 40000

N D Hopcroft RR, Roff JC, Chavez FP (2001) Size paradigms in copepod communities: a re-examination. Hydrobiologia 453:133-141 and higher trophic levels. This may be especially important in oligotrophic h th D eb 6t b 20th N F e Mar 4th D Apr 8th Jul 15th D ep 11th N Oct 6 Dec 9th N Jan 13th D Jan 27th N F Mar 18th N May 5th DJun 11th N Aug 11th DS Nov 14th D 35000 regions of the world’s oceans such as the Sargasso Sea. Legendre L, Rivkin RB (2002) Fluxes of carbon in the upper ocean: regulation by food-web control nodes. Marine Ecology-Progress 30000 Other non-calanoids Series 242:95-109 Total Copilia 25000 Total Sapphirina Total Harpacticoids Longhurst AR, Bedo A, Harrison WG, Head EJH, Horne EP, Irwin B, Morales C (1989) Nflux - a Test of Vertical Nitrogen Flux by 20000 Total Lubbockia Total Corycaeus Diel Migrant Biota. Deep-Sea Research Part a-Oceanographic Research Papers 36:1705-1719 Diel Changes Total Farranula 15000 Total Oncaea Total Oithona Ohtsuka SK, N; Okada, M; Gushima, K (1993) Attachment and feeding of pelagic copepods on larvacean houses. Journal of 10000 Materials and methods meter per individuals of squared Number Diel variability was investigated by using data generated from analysis of day-night Oceanography 49:115-120 1999 BATS non-calanoid copepod abundance 5000 pairs from each cruise. Paired samples t-tests at an alpha set at 0.05 were employed Omori M, Ikeda T (1984) Methods in marine zooplankton ecology. New York : Wiley: 332 p. Zooplankton samples used in this study were gathered as described in Madin et al. 30000 0 d N D D h h nd N nd D 2 2 p 8t to test for significant differences. b 11th Db 28th D b 28th N Apr 8th Jul 8t e p 10th N to test for significant differences. e e Apr 7th Jun 3rd D e Mar 9th N Jun 2nd N S e Dec 8th D Jan 12thF N F F Mar 25th N Aug 11th D S Oct 2 Oct 2 Nov 18thNov N 19th D (2001). The following is a brief summary of the methods used. Zooplankton were 25000 O'Neil JM (1998) The colonial cyanobacterium Trichodesmium as a physical and nutritional substrate for the harpacticoid copepod collected at the BATS site in the Sargasso Sea (31º 50’ N, 64º 10’W) on a semi- Macrosetella gracilis. Journal of Plankton Research 20:43-59 20000 Other non-calanoids O'Neil JM, Metzler PM, Glibert PM (1996) Ingestion of N-15(2)-labelled Trichodesmium spp and ammonium regeneration by the Most species analyzed for possible diel variation showed none. However, there were Total Sapphirina monthly basis employing a 1m2 rectangular net with 202µm mesh. Replicate day Total Copilia harpacticoid copepod Macrosetella gracilis. Marine Biology 125:89-96 Total Harpacticoids some notable exceptions. The Harpacticoid Distioculus minor showed significantly Total Lubbockia 15000 Total Corycaeus and night tows were made to a target depth of 200m. The net was fitted with a Total Farranula Paffenhofer GA, Knowles SC (1979) Ecological Implications of Fecal Pellet Size, Production and Consumption by Copepods. Journal greater abundance at night (p=0.028). However, since the abundance of this species Total Oncaea Total Oithona flow-meter (General Oceanics) as well as time temperature and depth recorder 10000 of Marine Research 37:35-49 was generally low (16 vs 8 ind m-2 for night and day ,respectively). meter square per individuals Number of (Vemco Minilog recorder) from June 1995 onwards. Prior to June 1995 depth was 5000 Roman MR (1978) Ingestion of Blue-Green-Alga Trichodesmium by Harpactacoid Copepod, Macrosetella-Gracilis. Limnology and Oceanography 23:1245-1248 Roman MR (1978) Ingestion of Blue-Green-Alga Trichodesmium by Harpactacoid Copepod, estimated from the wire out and the wire angle. Average depth sampled was 194m Another group that exhibited statistically significant diel differences in abundance Another group that exhibited statistically significant diel differences in abundance 0 Macrosetella-Gracilis. Limnology and Oceanography 23:1245-1248 (range = 93-292m). Volume filtered was estimated from the flow-meter counts and Jul 6th D Jul 6th N Jul 5th Jun 1st N Jun 1st Apr 7th D Apr 7th N Apr 8th Dec 8th N Dec 8th Aug 3rd N Aug 3rd Dec 9th D Dec 9th May 3rd N May 3rd May 3rd D May 3rd Jan 14th N Jan 14th N Jan 29th

were the Corycaeidae. Corycaeus typicus and C. limbatus males exhibited significant N Oct 11th Jan 15th D Jan 15th D Jan 27th D Oct 12th

were the Corycaeidae. Corycaeus typicus and C. limbatus males exhibited significant N Nov 10th Feb 12th N Feb 12th N Mar 23rd D Nov 10th Sep 14th N Sep 14th Feb 23rd N Feb 23rd Sep 15th D Sep 15th Mar 23rd D Mar 23rd the mouth area of the net corrected to an effective mouth area and averaged 635 thFeb 24 D Small LF, Fowler SW, Moore SA, Larosa J (1983) Dissolved and Fecal Pellet Carbon and Nitrogen Release by Zooplankton in diel patterns (p= 0.03 and 0.02, repectively). Tropical Waters. Deep-Sea Research Part a-Oceanographic Research Papers 30:1199-1220 m3 with a minimum of 246 and maximum of 2345 m3. Interannual Variability Steinberg DK, Carlson CA, Bates NR, Goldthwait SA, Madin LP, Michaels AF (2000) Zooplankton vertical migration and the active Zooplankton from the tows were split into 2 parts with one part wet sieved Finally, the strongest diel patterns were observed in 2 Oncaea species. They were transport of dissolved organic and inorganic carbon in the Sargasso Sea. Deep-Sea Research Part I-Oceanographic Research Papers and frozen for biomass determinations and the other half was used to make a Oncaea conifera and O. mediterranea. Both species displayed significant diel There were no significant differences between years in terms of the abundance of the 47:137-158 silhouette photograph and then preserved in 5% buffered formalin changes in abundance with much higher numbers taken at night in the upper 200m various non-calanoid copepod groups. However, given that the lower power Steinberg DK, Carlson CA, Bates NR, Johnson RJ, Michaels AF, Knap AH (2001) Overview of the US JGOFS Bermuda Atlantic solution. than during the day at the BATS Station (p = 0.02 for O. mediterranea and p<< nonparametric Kruskal-Wallis test was used true differences may have been masked. Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep-Sea Research Part Ii-Topical Studies in Oceanography 48:1405-1447 For this study, preserved samples representing 118 tows were analyzed. In general 0.001 in O. conifera’s case). The implications of this diel migration could have When more samples are analyzed such that the sample sizes become balanced then 1/32 of the preserved sample was used (range = 1/8 -1/256). ecological significance for carbon and nitrogen cycling at BATS. more powerful parametric tests such as ANOVA will be utilized in the analysis of Zhang X, Dam HG, White JR, Roman MR (1995) Latitudinal Variations in Mesozooplankton Grazing and Metabolism in the Central Tropical Pacific During the Us Jgofs Eqpac Study. Deep-Sea Research Part Ii-Topical Studies in Oceanography 42:695-714 Non-calanoid Families and Species identified at BATS interannual differences that may show some interannual trends.