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JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 12 j PAGES 1479–1488 j 2004 Summer coastal zooplankton biomassand copepod community structurenear the Italian Terra Nova Base(Terra Nova Bay, Ross Sea, Antarctica) LUIGI PANE1*, MIRVANA FELETTI2, BARBARA FRANCOMACARO1 AND GIAN LUIGI MARIOTTINI11DIPARTIMENTO DI BIOLOGIA SPERIMENTALE, AMBIENTALE ED APPLICATA, UNIVERSITA` DI GENOVA, VIALE BENEDETTO XV, 5, I-16132 GENOVA, ITALY AND REGIONE LIGURIA, ASSESSORATO AGRICOLTURA E TURISMO, VIA FIESCHI 15, I-16121 GENOVA, ITALY Received April 8, 2004; accepted in principle 14 July, 2004; accepted for publication August 9, 2004; published online 31 August, 2004 The structure of the zooplankton biotic community and of copepod population in the coastal area ofTerra Nova Bay (Ross Sea, Antarctica) was investigated during the 10th Italian Antarctic Expedition (1994/1995). Zooplankton biotic community consisted mainly of pteropods (Limacina helicina andClione antarctica), Cyclopoid (Oithona similis), Poecilostomatoid (Oncaea curvata) and Calanoid(Ctenocalanus vanus, Paraeuchaeta antarctica, Metridia gerlachei and Stephos longipes) copepods,ostracods, larval polychaetes and larval euphausiids. Zooplankton abundance ranged from 48.1 ind mÀ3to 5968.9 ind mÀ3, and copepod abundance ranged from 45.2 ind mÀ3 to 3965.3 ind mÀ3. Thehighest peak of zooplankton abundance was observed between 25 m and the surface and was mainlydue to the contribution of O. similis, O. curvata and C. vanus. Zooplankton biomass ranged from5.28 mg mÀ3 to 13.04 mg mÀ3 dry weight; the maximum value was observed between 25 m andthe surface. Total lipid content varied from 216.44 to 460.73 mg gÀ1 dry weight.
Burghart et al. (1999) observed that the dynamics of mar- The zooplankton community of some Antarctic areas has ginal ice zone strongly affects the development of Antarctic been the subject of extensive investigations carried out near South Georgia Island (Pakhomov et al., 1997) and in Terra Nova Bay waters show peculiar physicochemical the Weddell Sea (Vuorinen et al., 1997; Burghart et al., features within the Ross Sea system, because summer heat- 1999). Studies on taxonomy, distribution and biomass of ing and the particular meteorological conditions can cause copepods have been carried out in the Ross Sea and in its temperature increase of surface levels up to 2C; heating can coastal zones, such as in McMurdo Sound (Bradford, induce also the stratification of high-salinity surface waters, 1971; Bradford and Wells, 1983; Hopkins, 1987); in high nutrient uptake by phytoplankton and increased phy- Terra Nova Bay and in its neighbouring areas, researches toplankton production (Catalano et al., 2000). For this rea- have been performed during the last decade (Carli et al., son, in Terra Nova Bay, two summer phytoplankton blooms 1990, 1992a,b, 2000; Guglielmo et al., 1990; Zunini occur, between December and January and in February Sertorio et al., 1990, 1992, 1994, 2000). Terra Nova Bay (Innamorati et al., 2000), the first of which is supported by is characterized by an extended polynya, and ice forma- Fragilariopsis cf. curta in the receding ice-edge zone and the tion–melting processes are supposed to affect the behav- second one by different species (Nuccio et al., 2000). Phyto- iour of planktonic organisms; in fact, ice is one of the plankton of Terra Nova Bay is patchily distributed (Arrigo main environmental factors affecting the growth of coastal and McClain, 1994), and some zones are dominated by sea-ice microalgae and the availability of suspended diatoms (Fragilariopsis and Nitzschia) and Phaeocystis sp., while particles in Antarctic upper coastal waters (Guglielmo dinoflagellates and other flagellates mainly dominate in less et al., 2000; Misic et al., 2002). In this connection, rich zones; anyhow, different phytoplankton assemblages doi:10.1093/plankt/fbh135, available online at Journal of Plankton Research Vol. 26 No. 12 Ó Oxford University Press 2004; all rights reserved JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 12 j PAGES 1479–1488 j 2004 seem to alternate during the summer in the different areas (Nuccio et al., 2000). Smaller-sized organisms (<2 mm) could The expedition to Terra Nova Bay (Ross Sea) was carried reach also $60% of total biomass and could be the main out from 21 January 1995 to 11 February 1995, during the component of microbial population; their occurrence seems 10th Italian Expedition in Antarctica 1994/95 in the frame- to be negatively related to the total plankton biomass; hence, work of the Italian National Program for Antarctic when the total biomass is high the picoplankton seems to Research (PNRA), ROSSMIZE (Ross Sea Marginal Ice decrease, while it increases when the microzooplankton Zone Ecology) project, with RV Italica. On the whole, 65 biomass decreases (La Ferla et al., 1995). An extensive zooplankton samples were collected in two stations (T1 and study concerning chemical and biological properties of T2) of the coastal area between 7441.9200 S and annual pack ice in Terra Nova Bay was carried out by 7442.3000 S latitude and between 16410.0500 E and Guglielmo et al. (Guglielmo et al., 2000).
16411.0000 E longitude in sea-ice proximity (Fig. 1), by Extreme environmental conditions have forced the using a standard WP2 net (mesh size 200 mm), equipped organisms living at these latitudes to develop different with two Hydro Bios digital flow meters, one of them placed adaptive strategies which involve their vertical distribution within the net mouth and the other one placed externally; and trophic structure and affect the whole plankton biotic net trawls were carried out by the motorboat Malippo. The community. For example, Eucalanidae and Calanidae bottom depth of sampling zone ranged from 250 to 450 m.
accomplish wide seasonal vertical migrations and Ctenoca- Samples were collected at four different depths: from 150 to lanus spp., Euchaeta spp. and Metridinidae show winter 100 m, from 100 to 50 m, from 50 to 25 m and from 25 m descent (Atkinson and Sinclair, 2000). Antarctic zooplank- to the surface; one surface horizontal trawl was also carried ton are also able to maintain active metabolism and out. In the base laboratory, samples were divided at once growth by using energy reserves such as lipids (Clarke into two aliquots of 250 mL each: the first one was lyophil- and Holmes, 1986; Conover and Huntley, 1991; Hagen, ized, conditioned (70C, 12 h) and weighed for the deter- 1999; Swadling et al., 2000; Hagen and Auel, 2001).
mination of the biomass and maintained at À80C As in Antarctic waters, copepods form the bulk of total until analysis was performed in Italy; the other one was mesozooplankton biomass; in order to understand theirbiological and biochemical adaptive strategies, it is impor-tant to study their distribution along the water columnand characterize the compounds they accumulate, such aslipids. In this connection, studies on lipid content ofAntarctic copepods were carried out in specimens col-lected in the Weddell Sea (Schnack-Schiel et al., 1991;Drits et al., 1993; Hagen et al., 1993, 1995; Donnelly et al.,1994; Kattner et al., 1994; Schnack-Schiel and Hagen,1994; Geiger et al., 2001; Schnack-Schiel, 2001; Voroninaet al., 2001), in Bellingshausen Sea (Cripps and Hill, 1998),near South Georgia (Ward et al., 1996a,b; Pakhomov et al.,1997; Ward and Shreeve, 1999) and in sub-Antarcticwaters (Attwood and Hearshaw, 1992; Alonzo et al.,2000), but to date few studies have considered the lipidsin Ross Sea zooplankton.
In Terra Nova Bay, the summer plankton is mostly composed of copepods, which are particularly abundantbetween 50 and 100 m depth; these organisms are a funda-mental link in the marine food web of Antarctic circumpolarwaters which are characterized by scarce amounts of krill.
In this article, the results of a study on the zooplankton collected in Terra Nova Bay (Ross Sea) during the 10thItalian Expedition (1994/95) are reported. The aim of thiswork was to determine zooplankton biomass and total lipidcomposition and to characterize the zooplankton commu-nity structure, taking into particular account copepods, toimprove knowledge of the adaptive strategies and of therole of zooplankton in the Antarctic food web.
Fig. 1. Sampling site in Terra Nova Bay (Ross Sea).
L. PANE ETAL. j ZOOPLANKTON AND COPEPODS IN TERRA NOVA BAY maintained in 4% borax-buffered formalin solution. Total completely absent in the upper layer (0–50 m). Both for lipid content was measured after extraction by chloroform– copepods and other mesozooplankton, a decrease of methanol (2:1 vol:vol), according to Bligh and Dyer (Bligh numeric density was recorded, passing from upper to and Dyer, 1959). Taxonomy was performed by optical lower layers (Fig. 3a and b); in fact, both copepods and microscopy; the classification of pteropods, polychaetes, other mesozooplankters showed the peak of abundance ostracods and euphausiids was to the genus level, while cope- between 0 and 25 m depth (mean density 2369.67 and pods were classified to the species level. In total, 2482 cope- pods were identified. Zooplankton structure was evaluated The copepod community (Fig. 4) was mainly composed in terms of abundance (ind mÀ3) of the species occurring of Oithonidae and Oncaeidae, which together reached 100% at sea surface and per cent values ranging from77.09 to 83.32 of total copepods at the other depths, andClausocalanidae (8.97–15.25%); other families (Calanidae, Euchaetidae, Metridinidae, Stephidae and Acartiidae) The main features of samples collected in Terra Nova made up a small fraction of the total copepod population, Bay are summarized in Table I. Table II summarized the reaching a maximum of 10.12% (100–150 m depth).
structure of zooplankton population. Pteropods, cope- Figure 5a and b show, respectively, the distribution with pods, ostracods, larval polychaetes and larval euphausiids were recognized. Copepods dominated the zooplankton The copepod population (Table II) was composed mainly community in all samples and occurred mainly in the of Oithona similis (12.7–1162.8 ind mÀ3) and Oncaea curvata upper 25 m (maximum 3965.3 ind mÀ3); they made up (9.5–1947.7 ind mÀ3), which were the dominant species and always the bulk of zooplankton community, and their occurred at all examined depths; otherwise, Ctenocalanus percentage ranged from 72.8 to 92.5% (Fig. 2). Among vanus (maximum 444.4 ind mÀ3), Stephos longipes (maximum other zooplankters, pteropods (Limacina helicina and Clione 56.6 ind mÀ3), Metridia gerlachei (maximum 2.8 ind mÀ3) and antarctica) were abundant in the 0–25 m layer, reaching a Calanoides acutus (maximum 0.7 ind mÀ3) occurred more maximum of 1397.6 ind mÀ3 (19.8% of total population).
rarely and sometimes were absent; Calanus propinquus, Para- Other groups showed low abundance with percentages euchaeta antarctica, Paralabidocera antarctica and Oithona frigida <5%; larval polychaetes occurred scarcely at all depths; were collected occasionally. Copepodids of Calanoides larval euphausiids were absent in five samples; ostracods sp. (maximum 209.6 ind mÀ3), Oithona sp. (maximum were occasionally found between 50 and 150 m and were 174.4 ind mÀ3), M. gerlachei (maximum 118.2 ind mÀ3), Table I: Features of samples collected in the coastal area of Terra Nova Bay during Januaryto February 1995 Table II: Zooplankton and copepod abundance (ind mÀ3) in collected samples f, female; m, male; I–V, copepodid stage.
depth (m)
Fig. 2. Per cent frequency of main zooplankton groups collected atthe various depths. Among ‘others’ ostracods, euphausiid larvae and Fig. 4. Per cent composition of copepods (by Family) at the different depths. ‘Others’ comprise Acartiidae, Stephidae, Metridinidae andEuchaetidae.


depth (m)
depth (m)
depth (m)
depth (m)
Fig. 5. Vertical distribution (ind mÀ3) of adult copepods (a) andcopepodids (b). Mean Æ SD.
Fig. 3. Abundance of copepods (a) and other zooplankton (b) (ind mÀ3)in relation to depth (mean Æ SD).
sp. (124.43 and 136.93 ind mÀ3 on average respectively)were particularly abundant. Copepod abundance was Ctenocalanus sp. (maximum 116.3 ind mÀ3), Oncaea sp.
observed to decrease in lower layers.
(maximum 64.8 ind mÀ3), Paraeuchaeta sp. (maximum Adult M. gerlachei, which are known to be particularly 48.5 ind mÀ3) and Stephos sp. (maximum 44.7 ind mÀ3) abundant in several Antarctic waters (Carli et al., 1990, 1992a), were scarce, with an abundance peak between 25 Figure 6 shows vertical distribution of the most frequent and 50 m (mean 1.23 ind mÀ3); furthermore, copepodids copepod species. The peak of copepod abundance of Metridia sp. were observed to increase with depth.
recorded between the surface and 25 m depth was mainly The value of total plankton biomass collected by hori- due to O. curvata (mean 1224.33 ind mÀ3) and O. similis zontal trawl at the surface was very low (0.88 mg mÀ3); (mean 822.23 ind mÀ3). In this layer, also C. vanus (mean furthermore, in this sample, the biomass was mainly com- 214.17 ind mÀ3) and larval stages of Calanidae and Oithona posed of phytoplankton (Fig. 7). As regards vertical JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 12 j PAGES 1479–1488 j 2004 Fig. 6. Vertical distribution (ind mÀ3) with depth (m) of the main copepod species (mean Æ SD).
samples, zooplankton biomass values showed a decrease bulk of zooplankton biomass was composed of small species with depth and ranged from 13.0 to 5.3 mg mÀ3; the lower (C. vanus, O. similis and O. curvata) and copepodids of value was recorded between 150 and 100 m, and the Ctenocalanus sp., Oithona sp. and Oncaea sp., whose inclusive maximum occurred between 25 m and the surface. The contribution to the total biomass ranged between 47.5% L. PANE ETAL. j ZOOPLANKTON AND COPEPODS IN TERRA NOVA BAY Nova Bay zooplankton, in particular the species Euphausiacrystallorophias (Hureau, 1994; Sala et al., 2002) and Pleura- gramma antarcticum (Guglielmo et al., 1998; Granata et al., 2000; Vacchi et al., 2002), were observed.
In Terra Nova Bay, the concurrence of some physical and hydrologic factors, such as water summer heating, sea- ice melting and low hydrodynamism, results in nutrient lipids (mg/g DW)
biomass (mg/m3)
concentrations that might be limiting for phytoplankton growth (Catalano et al., 2000). Nevertheless, an enhanced nutrient cycling can support a satisfactory primary produc- tion and phytoplankton growth; in consequence of these depth (m)
factors, the production of small-sized herbivore species is Fig. 7. Zooplankton biomass (mg mÀ3 dry weight) and lipids (mg gÀ1 made easier, particularly in the marginal ice zone. In this dry weight) at the different depths.
connection, as a high occurrence of small-size species hasbeen observed, it can be assumed that most of the Ross Sea (100–150 m depth) and 72.4% (25–50 m depth). The zooplanktonic copepods are phytoplanktivorous and that biomass of copepods for each depth was calculated con- their growth is supported by phytoplankton blooms occur- sidering the available data of individual dry weight (Zunini ring in early and late summer (Innamorati et al., 2000; Sertorio et al., 1990). Total lipid percentage on dry weight Nuccio et al., 2000), even if the ratios between phytoplank- varied from 24.6 (150–100 m) to 46.0 (50–25 m); it showed ton biomass and nutrient availability are low due to high an increase from 25 to 50 m depth and a subsequent nutrient concentrations (Innamorati et al., 2000). Further- more, as several species are omnivores, microzooplanktonthat are particularly abundant in this area (Fonda Umaniand Monti, 1990) also play an important role in their diet.
In vertical samples collected from 150 m depth to the In the examined samples, copepods made up the bulk of surface, the bulk of mesozooplankton biomass was com- neritic zooplankton of Terra Nova Bay, as previously posed of C. vanus, O. similis and O. curvata and copepodids of reported (Guglielmo et al., 1990; Hecq et al., 1990). Pteropods the same genera, which reached 72.4% of total sampled and larval polychaetes were fairly abundant, while the other zooplankton from 50 to 25 m depth. The use of the WP2 zooplankters occurred scarcely. The highest mesozooplank- net with 200 mm mesh did not enable a quantitative sam- ton abundance and the peak of copepods were recorded pling of large-sized planktonic organisms, such as larval between the surface and 25 m depth. Few copepod species and adult euphausiids and larval fish; in general, biomass were recognized: all of them are typical of Antarctic coastal values recorded during this study are lower than those waters and of Terra Nova Bay (Bradford, 1971; Zvereva, reported during sampling by a bongo net (0.3 mm mesh) 1972; Schnack, 1985; Carli et al., 1990, 1992a,b; Zunini near South Georgia (Pakhomov et al., 1997) and in the Sertorio et al., 1990, 1992; Conover and Huntley, 1991).
Atlantic Sector of the Southern Ocean (Pakhomov et al., In comparison with data obtained by several scientists 2000). Otherwise, excepting the value recorded at 0–25 m who collected zooplankton by using different strategies depth, our results are comparable with those obtained by [bongo nets, Bedford Institute of Oceanography Net using the same sampling strategy near South Georgia Environmental Sampling System (BIONESS), WP3 and (Pakhomov et al., 1997) and by rectangular midwater trawls Hamburg Plankton Net (HPN)], with the sampling systems (RMT) in the Weddell Sea (Boysen-Ennen et al., 1991).
we used (WP2 net) the plankton was dominated by small- Furthermore, also considering that, to our knowledge, size species, such as O. similis and O. curvata, which domi- data of zooplankton biomass sampled with a WP2 net are nated the copepod community, and C. vanus; similar results not available for Terra Nova Bay, this sampling strategy were reported by Ossola and Licandro (Ossola and Licandro, allowed us to collect small-sized specimens (larval and adult 1997) who examined the samples collected in Terra Nova copepods), while sampling carried out by using other sys- Bay under the ice, during the following Italian Expedition tems, such as BIONESS, is best for elucidating the biomass (1995–96) using nets equipped with meshes of the same of greater zooplanktonic organisms. In fact, M. gerlachei, size. Anyhow, these species are known to be representative C. acutus and P. antarctica were scarcely sampled even if they of and abundant in Antarctic waters (Bradford, 1971). In are known to be abundant in Terra Nova Bay and in this connection, owing to the sampling procedure, in our neighbouring areas, and they occurred mainly in samples samples only few euphausiid larvae and no larval fish, collected by nets of larger mesh size than those used in the which are known to be an important portion of Terra present study (Carli et al., 1990, 1992a,b, 2000; Hecq et al., JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 12 j PAGES 1479–1488 j 2004 1990). It can be supposed that the coast proximity can also in agreement with that reported in previous studies con- have an influence on the sampling of these species (Ossola cerning the main Antarctic species (Conover and Huntley, and Licandro, 1997). Notwithstanding the above, small 1991; Kattner et al., 1994; Schnack-Schiel and Hagen, 1994; calanoids and cyclopoids dominate in several sites. Their Hagen et al., 1995). Hagen et al. (Hagen et al., 1993) observed role in the zooplankton community is often underestimated that C. acutus stores lipids in oil sacs, which are accumulated (Errhif et al., 1997), although small species are important for when food availability is plentiful; furthermore, lipid storage both their absolute number and grazing impact on primary supports phytoplanktivorous organisms, which otherwise producers. The dominance of O. similis, O. curvata and C.
should be affected by the marked seasonality of phytoplank- vanus in our samples suggests their high adaptability to ton growth, typical of Antarctic waters. Consequently, even trophic and hydrologic conditions. In this connection, if these species were quite scarce between 25 and 50 m depth although most studies on Antarctic copepods have concen- as compared with other copepods, their contribution to total trated on large species, these results suggest that also smal- ler copepods such as Oithona, Oncaea and Ctenocalanus are It is well known that zooplankton and in particular important, with the grazing impact of small species often phytoplanktivorous copepods play a fundamental role in exceeding that of larger copepods (Atkinson and Sinclair, energy transfer along the Antarctic food web, and krill 2000). Furthermore, small species are often underesti- and copepods are known to be the main food source for mated in samples collected by >200 mm mesh nets, marine mammals and birds in the Southern Hemisphere because of the escape of early copepodids; for example, (Reid et al., 1997; Barlow et al., 2002; Reid, 2002). In this the contribution of Oithona spp. to total copepod amount connection, Falk-Petersen et al. (1999) observed that the varies, in general, between 40 and 50% in samples col- highly efficient energy transfer occurring during the short lected by 100–200 mm mesh nets (Atkinson, 1998).
polar summer is due to energy production accomplished Zooplankton biomass was seen to decrease with depth by polar phytoplankton blooms that is transferred, to a and showed its highest value between the surface and 25 m, large extent as lipids, through the phytoplanktivorous where the peak of zooplankton, and in particular of zooplankton to marine predators. In addition, polar zoo- small copepods, occurred. As copepods were the dominant plankton synthesizing wax esters as energy reserve is a fraction of total mesozooplankton, our data are comparable major adaptation to the Antarctic conditions (Albers et al., with those obtained by Zunini Sertorio et al. ( Zunini Sertorio 1996). This environment is characterized by short periods et al., 1994) in the same area. High values of biomass in of intense primary production followed by long periods of upper layers, in particular between 0 and 50 m depth, can be low production. Therefore, biochemical processes gener- ascribed to the occurrence of phytoplanktivorous zooplank- ating oil reserves enable species to utilize different ecolo- ton, and biomass decrease along the water column can be gical niches and are fundamental to a determination of due to the scarce occurrence of the large-sized, carnivorous the biodiversity in Antarctic mesozooplankton (Falk- copepod P. antarctica and of omnivorous species such as M. gerlachei whose abundance decreases in deepest layers.
On the whole, this study shows that in the coastal zone On the contrary, the total lipid percentage by dry weight of Terra Nova Bay copepods dominate markedly the showed its maximum between 25 and 50 m depth, in con- zooplankton biotic community even if they occur with nection with the highest abundance of M. gerlachei and few species. Furthermore, the dominance in the copepod copepodids of Paraeuchaeta sp. and with the noticeable occur- community of small-sized species O. similis and O. curvata rence of C. acutus, which are known to store large amounts of suggests a high degree of adaptability to the environmen- lipids (Albers et al., 1996; Hagen and Schnack-Schiel, 1996; tal and trophic conditions; this is particularly true for Geiger et al., 2001; Voronina et al., 2001).
O. curvata, which has been described as indicative of sea-ice Falk-Petersen et al. (Falk-Petersen et al., 1999) observed proximity (Errhif et al., 1997). In conclusion, the domi- that lipids originating from phytoplankton are abundant in nance of small copepods over large-sized species, such as high-latitude marine organisms and play a key role as several calanoids typical of Antarctic waters, suggests that energy reserve; in fact, in polar waters, lipid levels reach their role in the zooplankton community could be under- up to 40–70% of dry weight in largest copepods and estimated (Chahsavar-Archad and Razouls, 1982), and euphausiids. For example, C. acutus adult females show their abundance can be fully appreciated by using fine dry weight lipid percentages varying from 35 in winter to mesh nets (Atkinson and Sinclair, 2000).
51 in summer (Schnack-Schiel et al., 1991; Hagen et al.,1993; Falk-Petersen et al., 1999), P. antarctica reaches values up to 42% and M. gerlachei shows percentages ranging from21 in summer to 40 in autumn (Schnack-Schiel et al., 1991).
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