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Boletín de Investigaciones Marinas y Costeras - INVEMAR

Print version ISSN 0122-9761

Bol. Invest. Mar. Cost. vol.48 no.1 Santa Marta Jan./June 2019  Epub Aug 30, 2019

https://doi.org/10.25268/bimc.invemar.2019.48.1.754 

Research Articles

Mesozooplankton biomass and epipelagic copepod assemblages in the Gerlache Strait (Antarctica) during the 2015 austral summer

Alan Giraldo1 
http://orcid.org/0000-0001-9182-888X

Maria Isabel Críales-Hernández2 
http://orcid.org/0000-0001-5608-8943

Mauricio Jeréz-Guerrero2  1 
http://orcid.org/0000-0002-2408-4849

Diego F. Mojica-Moncada3 
http://orcid.org/0000-0002-5570-7527

1 Universidad del Valle, Facultad de Ciencias Naturales y Exactas, Departamento de Biología, Grupo de Investigación en Ciencias Oceanógraficas. Cali. alan.giraldo@correounivalle.edu.co, oceanografia@correounivalle.edu.co ID: 0000-0001-9182-888X.

2 Universidad Industrial de Santander, Escuela de Biología, Laboratorio de Hidrobiología, Grupo Centro de Estudios e Investigaciones Ambientales. Bucaramanga. mcrialis@uisedu.co, jerez.guerreromauricio@gmail.com ID: 0000-0001-9182-888X, ID: 0000-0001-9182-888X.

3 Comisión Colombiana del Océano. Asesor de Asuntos Antárticos. Bogotá. Institución actual: Centro de Investigaciones Oceanográficas e Hidrográficas, Dirección General Marítima. Cartagena de Indias. asuntosantarticos@gmail.com ID: 0000-0002-5570-7527.


ABSTRACT

Mesozooplankton biomass and epipelagic copepod assemblage composition and distribution were studied in the Gerlache Strait from January 17 to 22, 2015, as part of the first Colombian oceanographic expedition to the Antarctic. Mesozooplankton-integrated biomass was generally low (< 5 mg dry weight / m-2) in the outer area of the northern section of the Gerlache Strait (between Crocker Passage and Hughes Bay) although there was a notable increase southward, with the highest value (1.02 g dry weight / m-2) at the entrance of Wilhelmina Bay in the central zone of the Strait. The epipelagic copepod assemblage comprised 17 species belonging to 4 orders and 13 families. The dominant species by number was Oithona similis, followed by O. frigida, Ctenocalanus citer, Drescheriella glacialis, and Calanoides acutus. Aetideus armatus is reported for the first time in the western sector of the Antarctic Peninsula. Differences in the assemblages of copepods between the northern and southern section of the Gerlache Strait were established. Considering the previous results reported about hydrography and phytoplankton composition in Gerlache Strait and our analysis of the copepod assemblage structure, a scenario is suggested in which, at less during January 2015, each section of the Strait exhibited a particular copepod assemblage structure: a northern section was dominated by small-sized copepods while the southern section was dominated by small-sized and large-sized copepods.

KEYWORDS: Aetideus armatus; Antarctic Peninsula; Bellingshausen Sea; Oithona similis; Zooplankton

RESUMEN

Se estudió la biomasa del mesozooplancton y la composición y distribución del ensamblaje de copépodos epipelágicos en el Estrecho de Gerlache entre el 17 y el 22 de enero de 2015, como parte de la primera expedición colombiana a la Antártica. La biomasa integrada del mesozooplancton generalmente fue baja (<5 mg peso seco /m-2) en el área externa de la sección norte del Estrecho de Gerlache (entre el paso Crocker y la bahía Hughes) aunque hubo un notable incremento hacia el sur, con el mayor valor de biomasa (1,02 g peso seco /m-2) en la entrada de la bahía Wilhelmina, área central del estrecho. El ensamblaje de copépodos epipelágicos estuvo conformado por 17 especies, de 4 órdenes y 13 familias. La especie dominante en número fue Oithona similis, seguida por O. frigida, Ctenocalanus citer, Drescheriella glacialis y C. acutus. Se registra por primera vez Aetideus armatus en el sector occidental de la península Antártica. Se establecieron diferencias en los ensamblajes de copépodos entre la sección norte y la sección sur del Estrecho de Gerlache. Considerando los resultados previamente registrados acerca de la hidrografía y la composición del fitoplancton en el Estrecho de Gerlache y el análisis sobre la estructura del ensamblaje de copépodos, se sugiere un escenario en el que, al menos durante enero de 2015, cada sección del estrecho presentó un ensamblaje particular de copépodos: una sección norte que estuvo dominada por copépodos de talla pequeña mientras que la sur estuvo dominada por copépodos de talla pequeña y grande.

PALABRAS CLAVE: Aetideus armatus; Mar de Bellingshausen; Península Antártica; Oithona similis; Zooplancton

INTRODUCTION

The Gerlache Strait is part of the shelf region of the Western Antarctic Peninsula. Winds and storms have little influence over this area, and freshwater input due to melting increases the stability of the surface of the water column, which leads to increased productivity (Holm-Hansen and Mitchell 1991, Smith Jr et al. 1987, Smith et al. 1996, Lancelot et al. 1993, Isla et al. 2002, Varela et al. 2002, Ducklow et al. 2012). This area has been considered by different authors as main foraging area for numerous taxonomic groups, and has therefore been of permanent interest for Antarctic research (Hopkins et al 1985, Brinton 1991, Huntley and Brinton 1991, Huntley et al. 1991, Whitehouse and Veit . 1994, Zhou et al. 1994, Fraser and Trivelpiece 1996, Ross, et al. 1996, Silva et al. 2001, Cabal et al. 2002).

Taking into account the classification of Antarctic marine biomes developed by Treguer and Jacques (1992), the Gerlache Strait is part of the continental platform ecosystem, which is characterized by having high phytoplankton biomass levels during spring and summer (Smith Jr and Nelson 1986, Holm-Hansen and Mitchell 1991, Varela et al. 2002, Ballerini et al. 2014). In addition to krill, one of the taxonomic groups that take advantage of phytoplankton availability in this region are copepods, with a feeding impact of up to 65% of daily local primary production, and a re-directing through fecal pellets of over 22% of total organic carbon flow in the area (Gleiber et al. 2012). These characteristics mean that copepods are a key taxonomic group in the dynamics of the pelagic ecosystem of this region (Gleiber et al. 2016).

The Western Antarctic Peninsula, where the Gerlache Strait is located, is one of the locations where the highest rate of thermal change due to global warming has been recorded on the planet (Vaughan et al. 2003). This thermal variation has led to a significant change in the structure of all taxonomic levels of the pelagic trophic web (Montes-Hugo et al. 2008, Stammerjohn et al. 2008). In particular, the analysis of time series of zooplankton composition indicates that copepod abundance in this region has increased significantly over the last two decades (Ross et al. 2008, 2014, Steinberg et al. 2015). This change could have a significant effect on the efficiency of the biological pump (Steinberg et al. 2012). There has even been evidence that the western side of the Antarctic Peninsula has changed from being a system dominated by herbivorous euphausiids, to a system dominated by herbivorous microzooplankton (Sailley et al. 2013). In this new scenario copepods would serve as a direct link between the two systems described, due to their flexible feeding strategy that allows them to browse on diatoms or on microzooplankton (Gleiber et al. 2016).

In the Gerlache Strait, our knowledge of epipelagic copepod communities remains limited. Therefore, in the present study, we report on mesozooplankton biomass and the structure of the epipelagic copepod assemblage in the Gerlache Strait during the 2015 austral summer.

MATERIALS AND METHODS

The area of study

The general topography and hydrography of Gerlache Strait has been summarized by García et al. 2002 and Zhou et al. (2002, 2006). The Gerlache Strait is located on the west side of the Antarctic Peninsula, between the Palmer Archipelago and the Danco Coast. It is almost 200 km long with 50 km wide on the northern end and 10 km wide on the southern, and forms the deepest western connection between the Bellingshausen Sea (BS) and Bransfield Strait (BSt) (Figure 1). However, near to the southwest entrance, the Gerlache Strait has sill shallower than 350 m that restrict the influence of largescale circumpolar flow.

Figure 1 Map of the study area showing the sampling stations for zooplankton in the Gerlache Strait during the I Colombian Antarctic Expedition. The dotted line divides the Gerlache Strait into a northern section (stations 1 to 11, including station 15), and a southern section (stations 12 to 20, excluding station 15). BS: Bellingshausen Sea, BSt: Bransfield Strait, SC: Schollaert Channel, FB: Flanders Bay, WB: Wilhelmina Bay, HB: Hughes Bay, CP: Crocker Passage. 

The typical water column at the southwestern part of the Gerlache Strait is dominated by Antarctic surface water and an underlaying local circumpolar Deep Water, while in the northeast part consist of an upper layer of transitional zonal waters with Bellingshausen Sea influence and an underlaying of transitional zonal waters with Weddell Sea influence, with limited intermediate intrusion of local circumpolar Deep Water (García et al., 2002). The main surface current is the Gerlache Strait Current, that follows northeastward at the middle deep channel of the strait, exceeding 30 cm s-1. Its main flow, that feeds the Bransfield Strait Current, could advect a particle outside the GS in 7 to 10 days. However, in the shallow bay or around island of Gerlache Strait the particles would be trapped inside anticyclonic eddies for more to 70 days (Zhou et al. 2002, 2006, Jiang et al 2013).

Sample collection

We conducted zooplankton hauls in the Gerlache Strait between 17 January and 22 January 2015 aboard the "ARC 20 Julio" as part of the "Caldas Expedition", first expedition of the Colombian Antarctic program. Zooplankton for copepods analysis were collected at 20 station encompassing the northern and southern zone of the Gerlache Strait (Figure 1) with an oblique net tows within the upper 100 m using a 0.7 m circular frame net with 200 mm mesh, equipped with one Hydro Bios digital flow meter and non-filtering cod end. Towing speed was about 3 knots and filtered water volumes were calculated, considering net speed and flow data. On board, zooplankton samples were preserved in 4% borax-buffered formalin solution until analysis was performed in Colombia. Vertical profiles of temperature and salinity were taken with a SeaBird® CTD-19 and CTD-25 attached to a carrousel system.

Sample Analysis

A total of 20 samples were analyzed. The formaldehyde-preserved samples were split, and one quarter of the sample was used to copepod sorting and another quarter was used to determine zooplankton biomasses by drying batches at 60°C and weighing on a microbalance (0.0001 g) (Postel et al., 2000). These values were then multiplied by 1.25 as an adjustment for tissue loss in formaldehyde (Hopkins 1971). Taxonomy was performed by optical microscopy and the copepods were classified to the species level (Razouls et al., 2019). Graphs of the spatial variation of zooplankton biomass, total copepod abundance (taking into account developmental stages), and abundance of each species identified in the study area were carried out.

A graphic representation of the thermal and hyaline structure of the Gerlache Strait during the sampling period was created by interpolation using the kriging method in the Surfer® program. Taking into account the geomorphological and hydrodynamic conditions described for the Gerlache strait by Zhou et al. (2002), as well as the thermal and hyaline structure of the superficial layer of the water column during sampling period, the strait was divided into two sections: a northern section that communicates directly with the Bransfield Strait and a southern section that has a restricted connection with the Bellingshausen Sea (Figure 1), in order to compare the temperature, salinity, mesozooplankton biomass and copepod abundance in the upper 100m of water column a Mann-Whitney comparison test (MW) was carried out.

Ensemble structure was evaluated in terms of abundance (ind 1000 m-3) of the species occurring in samples with a Whittaker rank/abundance graph (Krebs, 1999). Furthermore, a similarity matrix was constructed based on the log-transformed abundance data (Log10 X +1). Transformation was used to down-weight the importance of the dominant species and to increase the weighting of rarer ones (Clarke and Warwick, 2001). A similarity analysis (ANOSIM) was carried out to establish the significance of a priori grouping (Clark 1993, Clarke and Warwick, 1994). Additionally, ordination analysis of non-metrical multidimensional scaling (MDS) was performed to graphically represent the relations of the structure of the assemblages (Clarke and Ainsworth 1993). Taking into account the clusters established by prior analysis, a Simper analysis was performed to determine which species contributes to the similarity within each group and dissimilarity between groups (Clarke and Warwick, 2001). These analyses were performed using Primer® software.

RESULTS

Temperature and salinity condition of study area

Median water temperature from 0 to 100 m depth was significantly higher in the northern than in the southern section of the Gerlache Strait during the sampling period. Furthermore, water column sampled in the northern section was thermally stratified, with a range of thermal variation equivalent to 1.2 °C, while in the Southern section was thermally homogeneous with only 0.2°C range of variation between 0m to 100 m depth (Figure 2). Median water salinity from 0 to 100 m depth was similar in both sections of Gerlache Strait. Moreover, below of 30 m depth, the water column exhibited strong saline stratification conditions in both sections. However, in the southern section of Gerlache Strait surface water with low salinity were detected (Figure 2).

Figure 2 Spatial variation in temperature (°C) and salinity (UPS) in the superficial zone (0 to 100 m) of the water column along a longitudinal axis in the Gerlache Strait during the I Colombian Antarctic Expedition. The dotted line divides the strait into a northern (right) and southern (left) sections. Median value of temperature and salinity in each section of Gerlache Strait is reported. 

Mesozooplankton Biomass and Copepod Abundance

Average mesozooplankton biomass was 125.89 ± 82.07 mg dry weight / m2 in the Northern section of Gerlache Strait and 123.98 ± 44.29 mg dry weight / m2 in the Southern section of Gerlache Strait. No significant differences in mesozooplankton biomass were detected between section of Gerlache Strait (MW, Z = -1.23, p = 0.2380). However, the zooplankton biomass between Crocker Passage and Hughes Bay (outer Northern section) was one order of magnitude lower than in the stations near to Flanders Bay (outer Southern section), although the higher biomass (1.02. g dry weight / m2) was observed at the entrance of Wilhelmina Bay, in the central zone of Gerlache Strait (Figure 3A).

Figure 3 Spatial variation of zooplankton Biomass and Copepod abundance (Copepodite and Adults) in the Gerlache Strait during the I Colombian Antarctic Expedition. A. Biomass. B. Development stage. C. Adult Abundance. D. Copepodite abundance 

More than 92% of Copepods collected in both sections were adults (Figure 3B) and the proportion of stage development were no different between Northern and Southern sections (c2=55.2, p = 0.0001). The abundance of adult's copepods in the Northern section was one order of magnitude lower than in the Southern section of Gerlache Strait (MN, Z = - 2.78, p = 0.0055), being the higher abundances registered in the entrance of Schollaert Canal, which communicates the Gerlache Strait and the Bellingshausen Sea, and in the Flandres Bay, both locations in the Southern section of Gerlache Strait (Figure 3C).

Copepod Assemblage

A total of 17 copepod species belonging to four orders and 13 families were identified in the study area (Table 1). Copepodite stages, ranging from copepodite II (C2) to copepodite V (C5), were identified for Oithona similis (C2, C4, C5), Calanoides acutus (C2, C3, C4), Alteuta potter (C2, C3, C4), Subeucalanus mucronatus (C3, C4), Calanus propinquus (C4), and Clausocalanus laticeps (C4). However, only adult copepods were considered for assemblage structure analysis (Figure 4).

Table 1 Epipelagic copepods collected during the first Colombian Antarctic Expedition in the Gerlache Strait during the 2015 austral summer. ID: acronym. *Razouls et al. 2019

Figure 4 Structure and composition of the copepod assemblage in the epipelagic zone of the Gerlache Strait during the first Colombian Antarctic Expedition. 

In terms of abundance, the assemblage of the both sections in Gerlache Strait were dominated by Oithona similis (Figure 4). The abundance of this specie was one order of magnitude higher than Oithona frigida, Ctenocalanus citer, Drescheriella glacialis, and Calanoides acutus and three order of magnitude higher than Aetideus armatus, Calanus propinquus, Phaenna spinifera, Rhincalanus gigas, Subeucalanus. mucronatus, and Temora discaudata that were the least abundant copepod species in Gerlache Strati during sampling period (Figure 4, Figure 5).

Figure 5 Spatial variation of the most frequent (frequency > 50%) and abundant species of copepods in the epipelagic zone of the Gerlache Strait during the I Colombian Antarctic Expedition. 

Large multivariate differences in the structure of Copepod assemblages were apparent between sections of the Gerlache Strait (Figure 6). That is, assemblage on Southern section (Figure 6: black circles) are located to the upper-left of assemblages on Northern section (Figure 6: white circle) in the nMDS plot. Furthermore, pairwise comparisons suggested that the composition of copepod assemblages on Gerlache Strait differed significantly between Southern and Northern section (Anosim, R = 0.31, p = 0.01).

Figure 6 Non-metric multidimensional scaling (nMDS) plot of the epipelagic copepod assemblages in the Gerlache Strait during January 2015 (Northern section n = 12, Southern section n = 8). 

Comparisons of Bray-Curtis dissimilarity percentages (Simper test) supported this interpretation. Dissimilarities between Northern and Southern section of Gerlache Strait was 52%, generated by the contribution of O. frigida, C. acutus, D. glacialis, and C. citer (Table 2). Furthermore, Bray-Curtis similarity percentage in Southern section was 57.2% and in Northern section was 67.8% (Table 2).

Table 2 Specie contribution to similarity of the epipelagic copepods assemblage within the northern and southern sector of Gerlache Strait during austral summer of 2015. Dissimilarity among sectors is reported. 

DISCUSSION

With exception of Aetideus armatus, all copepod species registered in upper 100m of Gerlache Strait during summer 2015 have been previously reported from Antarctic Peninsula region (Hopkins 1985, Calbet et al. 2005, Gleiber 2014, Kouwenberg et al. 2014). This appear to be the first record of this species in the western region of Antarctica, specifically, in the southern section of the Gerlache Strait.

Average mesozooplankton biomass was in the range of the values cited in the literature for Western Antarctic Peninsula, including Bransfield and Gerlache Strait, in summer season (Hernández-León et al. 1999, 2000, Cabal 2002, Calbet et al. 2005). According to previous studies, the New Scotia Sea and shelf waters of Antarctic Peninsula is characterized by unexpectedly highly variable mesozooplankton biomass (Hérnandez-León et al. 2000, 2013, Cabal et al. 2002, Ward et al. 2004, 2005, Calbet et al. 2005, Gleiber 2014). Therefore, the low mesozooplankton biomass registered during early spring in the region would be indicated an delayed spring bloom in the region due to temporal variability of solar irradiance, variability in the upwelling of iron-reach subsurface water, seawater temperature increase or a variable sea-ice melting rate (Smith et al. 1998, Ducklow et al. 2007, Marrari et al. 2008).

Epipelagic copepod assemblage in Gerlache Strait appears quiet variable during January 2015, with a dominant species in common for all Strait, but suggestively different assemblage structure in each section. Oithona similis was numerically the most abundant species in all Gerlache Strait during sampling period. This species, has been reported in all Antarctic sectors like a dominant copepod in the upper part of water column. (Razouls et al., 2000; Giron, 2004; Ayón et al., 2007; Atkinson et al., 1996, 2012). In our samples, this species represented 80% of copepod relative abundance in all study area.

In addition to Oitona similis, the copepod assemblage in the Northern section was dominated by one small Ciclopoidae (Oitona similis) and another small Calanoidae species (Ctenocalanus citer) while in the Southern section of Gerlache Strait was dominated by two small Ciclopoidae species (Oitona similis and O. frigida), one species of Heparticoidae associated to sea ice (Drescheriella glaciales) and one large specie of Calanoidae (Calanus acutus). All small-sized pelagic copepod registered in our samples feed on microplankton. O. similis and O. frigida feeds preferably on microzooplankton ciliates and mobile microphytoplankton (Nishida, 1985; Eiane and Ohman, 2004; Calbet and Saiz, 2005; Atkinson et al., 2012), while C. citer feeds preferably on small-sized phytoplankton throughout the year (Pasternak and Schnack-Schiel, 2007). On the other hand, the large-sized copepod, C. acutus, has been traditionally viewed like a large-size mostly herbivorous specie of copepod and it is considered an important consumer of primary production in Antarctic waters (Huntley and Escritor 1991, Pasternak and Schanck-Schiel 2001, Calbet et al., 2006), while the smallsized copepod, D. glaciales, feeds on microphytobenthos and epiphytic diatoms that grows associated with sea ice (Schnack-Schiel et al. 2001).

Using data from summers of 1995 and 1996, Varela et al. (2002) described the Gerlache Strait as one of the most productive water bodies in the Antarctic peninsula, where primary production ranged between 0.87 and 4.54 g C m-2 d-1, chlorophyll a between 90 and 270 mg Chl a m-2, and microplankton (>10 μm) dominated the phytoplankton accounting for about 80% of total chlorophyll, whereas nanoplankton (2-10 μm) and picoplankton (0.2-2 μm) represented 7% and 15%, respectively, in the upper 50 m. This energy source, can be addressed by the large-sized herbivores zooplankton, as Calanoidae copepods, Salps or Krill (Hernández-León et al. 2001, Bernard et al. 2012, Lee et al. 2013) to support populations of top predators, such as seabirds, seals, and whales, and to inject particulate organic matter into deep water or benthic ecosystems via fecal pellets (Ducklow et al. 2007, Ross et al. 2008, Loeb and Santora 2012, Steinberg et al. 2012).

Recently, a shift in phytoplankton community composition from large diatoms to small flagellated cryptophytes has been reported for Bransfield Strait (Mendes et al. 2013) and Gerlache Strait (Mendes et al. 2018). According with our results, the dominance of small calanoids and cyclopoids over the large calanoids in the Gerlache Strait during summer 2015 suggests that their role in the energy flow of this locality may be underestimated. Small-sized copepods are not only important by their number but also by their grazing impact on primary production and on by their impact on microzooplankton flagellate populations (Froneman and Perissinotto 1996, Caron et al. 2000, Garzio and Steingerg 2013). Therefore, a transition from diatoms to cryptophytes represents a fundamental decrease in the size spectrum of the phytoplankton community, which would promote an increase in the abundance of small-sized copepods (Sailley et al., 2013, Gleiber 2014), as we reported for both sections of the Gerlache Strait.

In conclusion, based on data presented here, and considering the results reported by García et al. (2002), Zhou et al. (2002, 2006), Jiang et al. (2013), Varela et al. (2002), Rodríguez et al. 2002a, 2002b, Gonçalves-Araujo et al. 2015 and Mendes et al. (2018) about hydrography and phytoplankton composition of Gerlache Strait, we believe that copepod assemblage in this locality is being affected by specific conditions in each section of the Strait (e.g. thermic stratification, melting ice input, residence time, phytoplankton size composition and connection with adjacent seas), that may result in an copepod assemblage structure particular: a Northern section dominated only by small-sized copepods and a Southern section dominated by both, small-sized and large-sized copepods.

ACKNOWLEDGMENTS

We thank Marisol Rivera, Andrés Cuellar, Diego Córdoba, Isabel Cristina Calle, and Juan José Gallego for their help during the separation of biological samples. We thank the ARC 20 de Julio crew for their valuable collaboration during sampling and the Colombian Navy for allowing the use of the sampling platform. This study was co-financed by Universidad del Valle, Universidad Industrial de Santander, the Academia Colombiana de Ciencias Exactas, Físicas y Naturales, and the Colombian Commission of the Ocean (CCO) within the Colombian Antarctic Program.

REFERENCES

Atkinson, A., R.S. Shreeve, E.A. Pakhomov, J. Priddle, S.P. Blight and P. Ward. 1996 Zooplankton response to a phytoplankton bloom near South Georgia, Antarctica. Mar. Ecol. Prog. Ser., 144:195-210. [ Links ]

Atkinson, A ., P. Ward ., B.P.V. Hunt, E.A. Pakhomov and G.W. Hosie. 2012. An overview of Southern Ocean Zooplankton data: Abundance, biomass, feeding and functional relationships. CCAMLR Science, 19: 171-218. [ Links ]

Ayón, P, E. Pinedo y D. Lopez. 2007. Estructura comunitaria del zooplankton Antártico en el Estrecho de Bransfield y alrededores de la Isla Elefante, verano Austral 2007 ANTAR XVII. Bol. Inst. Del Mar del Perú., 31(1):121-127. [ Links ]

Ballerini, T., E. E. Hofmann, D. G. Ainley, K. Daly, M. Marrari, C. A. Ribic, W. O. Smith Jr. and J. H. Steele. 2014. Productivity and linkages of the food web of the southern region of the western Antarctic Peninsula continental shelf. Prog. Oceanogr., 122: 10-29. [ Links ]

Bernard, K. S., D. K. Steinberg and O. M. Schofield. 2012. Summertime grazing impact of the dominant macrozooplankton off the Western Antarctic Peninsula. Deep-Sea Res. Part I Oceanogr. Res. Pap., 62:111-122. [ Links ]

Brinton, E. 1991. Distribution and population structures of immature and adult Euphausia superba in the western Bransfield Strait region during the 1986-87 summer. Deep-Sea Res. Part II. Top. Stud. Oceanogr., 38: 1169-1194. [ Links ]

Cabal, J. A., F. Alvarez-Marqués, J. L. Acuña, M. Quevedo, R. Gonzalez-Quirós, I. Huskin, D. Fernandez, C. Rodríguez del Valle and R. Anadón. 2002. Mesozooplankton distribution and grazing during the productive season in the Northwest Antarctic Peninsula (FRUELA cruises). Deep Sea Res. Part II: Top. Stud. Oceanogr., 49(4-5): 869-882. [ Links ]

Calbet, A. and E. Saiz. 2005. The ciliate-copepod link in marine systems. Aquat. Microb. Ecol., 38: 157-167. [ Links ]

Calbet, A ., M. Alcaraz, D. Atienza, E. Broglio and D. Vaqué. 2005. Zooplankton biomass distribution patterns along the western Antarctic Peninsula (December 2002). J. Plankton Res., 27(11): 1195-1203. [ Links ]

Calbet, A ., D. Atienza , E. Broglio , M. Alcaraz and D. Vaque. 2006. Trophic ecology of Calanoides acutus in Gerlache strait and Bellingshausen Sea waters (Antárctica, diciembre de 2002). Polar Biol., 29(6): 510-518. [ Links ]

Caron, D. A., M. R. Dennett, D. J. Lonsdale, D. M: Moran and L. Shalapyonok. 2000. Microzooplankton herbivory in the Ross sea, Antarctica. Deep Sea Res. Part II: Top. Stud. Oceanogr . 47(15-16): 3249-3272. [ Links ]

Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol., 18: 117-143. [ Links ]

Clarke, K. R . and M. Ainsworth. 1993. A method of linking multivariate community. Mar. Ecol. Prog. Ser ., 92: 205-219. [ Links ]

Clarke, K. R . and R. M. Warwick. 1994. Similarity-based testing for community pattern: the two-way layout with no replication. Mar. Biol., 118(1): 167-176. [ Links ]

Clarke, K. R. and R. M. Warwick . 2001. Change in marine communities: an approach to statistical analysis and interpretation. Primer-E. Plymouth, UK. [ Links ]

Ducklow, H.W, K. Baker, D. G. Martinson, L. B. Quetin, R. M. Ross, R. C. Smith, S. E: Stammeriohn, M. Vernet and W. Fraser. 2007. Marine pelagic ecosystems: the West Antarctic Peninsula. Philos. Trans. R. Soc. Lond. B., 362: 67-94. [ Links ]

Ducklow, H.W ., A. Clarke, R. Dickhut, S. C. Doney, H. Geisz, K. Huang, D. G. Martinson , O. M. E. Schofield, S. E. Stammerjohn, D. K. Steinberg and W. R. Fraser. 2012. The marine system of the Western Antarctic Peninsula: 121-159. In: Rogers, A.D., N. M. Johnston, E. J. Murphy and A. Clarke (Eds). Antarctic Ecosystems: An Extreme Environment in a Changing World. Wiley-Blackwell, United States. 564 p. [ Links ]

Eiane, K. and M. D. Ohman. 2004. Stage specific mortality of Calanus finmarchicus, Pseudocalanus elongatus and Oithona similis on Fladen Ground, North Sea, during a spring bloom. Mar. Ecol. Prog. Ser ., 268: 183-193. [ Links ]

Fraser, W. R. and W. Z. Trivelpiece. 1996. Factors controlling the distribution of seabirds: winter-summer heterogeneity in the distribution of Adelie penguin populations. Antarct. Res. Ser., 70: 257-272. [ Links ]

Froneman, P. and R. Perissinotto. 1996. Microzooplankton grazing in the Southern Ocean: Implications for the carbon cycle. Mar Ecol, 17(1-3): 99-115. [ Links ]

García, M. A., C. G. Castro, A. F: Rios, M. D. Doval, G. Rosón, D. Gomis and O. López. 2002. Water masses and distribution of physico-chemical properties in the Western Bransfield Strait and Gerlache Strait during Austral summer 1995/96. Deep-Sea Res. Part II. Top. Stud. Oceanogr., 49(4): 585-602. [ Links ]

Garzio, L.M. and D.K. Steinberg. 2013. Microzooplankton community composition along the Western Antarctic Peninsula. Deep-Sea Res. Part I Oceanogr. Res. Pap ., 77: 36-49. [ Links ]

Giron, M. 2004. Zooplancton e ictioplancton antártico durante el verano Austral del 2003. Inf. Inst. del Mar del Perú., 32(4):359-363. [ Links ]

Gleiber M.R. 2014. Long-term change in copepod community structure in the Western Antarctic Peninsula: Linkage to climate and implications for carbón cycling. Master's thesis. Gloucester Point (VA): Virginia Institute of Marine Science, United States. 189 p. [ Links ]

Gleiber, M. R., D. K. Steinberg and H. W. Ducklow. 2012. Time series of vertical flux of zooplankton fecal pellets on the continental shelf of the western Antarctic Peninsula. Mar. Ecol. Prog. Ser ., 471: 23-36. [ Links ]

Gleiber, M. R ., D. K. Steinberg and O. M. Schofield . 2016. Copepod summer grazing and fecal pellet production along the Western Antarctic Peninsula. J. Plankton Res ., 38(3): 732-750. [ Links ]

Gonçalves-Araujo, R., M. S. de Souza, V. M. Tavano and C.A.E. Garcia. 2015. Influence of oceanographic features on spatial and interannual variability of phytoplankton in the Bransfield Strait, Antarctica. J. Marine Sys., 142: 1-15. [ Links ]

Hernández-León, S., S. Torres, M. Gomez, I. Montero and C. Almeida. 1999. Biomass and metabolism of zooplankton in the Bransfield Strait (Antarctic Peninsula) during austral spring. Polar Biol ., 21: 214-219. [ Links ]

Hernández-León, S . C., C. Almedia, A. Portillo-Hahnefeld, M. Gómez and I. Montero. 2000. Biomass and potential feeding, respiration and growth of zooplankton in the Bransfield Strait (Antarctic Peninsula) during austral summer. Polar Biol ., 23: 679-690. [ Links ]

Hernández-León, S ., A. Portillo-Hahnefeld , C. Almeida , P. Bécognée and I. Moreno. 2001. Diel feeding behavior of krill in the Gerlache Strait, Antarctica. Mar. Ecol. Prog. Ser ., 223: 235-242. [ Links ]

Hernández-León, S ., P. Sangrà, P. Lehette, L. Lubián, C. Almeida , S. Putzeys, P Becógnée and M. P. Andrade. 2013. Zooplankton biomass and metabolism in the frontal zones of the Bransfield Strait, Antarctica. J. Marine Sys ., 111: 196-207. [ Links ]

Holm-Hansen, O. and B. G. Mitchell. 1991 Spatial and temporal distribution of phytoplankton and primary production in the western Bransfield Strait region. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 38: 961-980. [ Links ]

Hopkins, T. L. 1971. Zooplankton standing crop in the Pacific Sector of the Antarctic. 347-362. In: Llano G.W. and I.E. Wallen (Eds.). Biology of the Antarctic Seas IV. Antarct. Res. Ser ., 362 p. [ Links ]

Hopkins, T. L. 1985. The zooplankton community of Croker passage, Antarctic Peninsula. Polar Biol ., 4(3): 161-170. [ Links ]

Huntley, M. E. and E. Brinton. 1991. Mesoscale variation in growth and early development of Euphausia superba Dana in the western Bransfield Strait region. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 38: 1213-1240. [ Links ]

Huntley, M. E . and F. Escritor. 1991. Dynamics of Calanoides acutus (Copepoda: Calanoida) in antarctic coastal waters. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 38: 1145-1167. [ Links ]

Huntley, M.E., D.M. Karl, PP. Niiler and O. Holm-Hansen. 1991. Research on Antarctic coastal ecosystem rates (RACER): an interdisciplinary field experiment. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 38: 911-941. [ Links ]

Isla, E., P. Masqué, A. Palanques, J.A. Sanchez-Cabeza, J.M. Bruach, J. Guillén and P. Puig. 2002. Sediment accumulation rates and carbon burial in the bottom sediment in a high-productivity area: Gerlache Strait (Antarctica). Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 49 (16): 3275-3287. [ Links ]

Jiang, M., M. A. Charette, C. I, Measures, Y. Zhu y M. Zhou. 2013. Seasonal cycle of circulation in the Antarctic Peninsula and the off-shelf transport of shelf waters into southern Drake Passage and Scotia Sea. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 90: 15-30. [ Links ]

Kouwenberg J. H. M., C. Razouls y N. Desreumaux. 2014.Southern ocean pelagic copepods. 290-296. In: De Broyer C., P. Koubbi, H. J. Griffiths, B. Raymond, C. d' Udekem-d'Acoz, A. P. Van de Putte, B, Danis, B, David, S. Grant, J. Gutt, C. Held, G. Hosie, F. Huettmann, A. Post and Y. Ropert-Coudert (Eds.). Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge. 49 8 p. [ Links ]

Krebs, C. J. 1999. Ecological Methodology. 2nd Ed. Benjamin Cummings. Menlo Park, CA, USA. 624 p. [ Links ]

Lancelot, C., S. Mathot, C. Veth, and H. W. de Baar. 1993. Factors controlling phytoplankton ice-edge blooms in the marginal ice-zone of the Northwestern Weddell Sea during sea ice retreat 1988FField observations and mathematical model. Polar Biol ., 13 (6): 377-387. [ Links ]

Lee, D. B., K. H. Choi, H. K. Ha, E. J. Yang, S. H. Lee, S. Lee and H. C. Shin. 2013. Mesozooplankton distribution patterns and grazing impacts of copepods and Euphausia crystallorophias in the Amundsen Sea, West Antarctica, during austral summer. Polar biol., 36(8): 1215-1230. [ Links ]

Loeb, V. J. and J.A. Santora. 2012. Population dynamics of Salpa thompsoni near the Antarctic Peninsula: growth rates and interannual variations in reproductive activity (1993-2009). Prog Oceanogr, 96(1): 93-107. [ Links ]

Marrari, M., K. L. Daly and C. Hu. 2008. Spatial and temporal variability of SeaWiFS chlorophyll a distributions west of the Antarctic Peninsula: Implications for krill production. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 55(3-4): 377-392. [ Links ]

Mendes, C.R.B., V. M. Tavano , M. C. Leal, M. S. de Souza , V. Brotas and C. A. E. García. 2013. Shifts in the dominance between diatoms and cryptophytes during three late summers in the Bransfield Strait (Antarctic Peninsula). Polar Biol ., 36: 537-547. [ Links ]

Mendes, C. R. B., V. M. Tavano , T. S. Dotto, R. Kerr, M. S. de Souza , C. A. E. García and E. R. Secchi. 2018. New insights on the dominance of cryptophytes in Antarctic coastal waters: a case study in Gerlache Strait. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 149 : 161-170. [ Links ]

49 " reftype=“journal">Montes-Hugo, M., M. Vernet , D. G. Martinson , R. Smith and R. A. Iannuzzi. 2008. Variability on phytoplankton size structure in the western Antarctic Peninsula (1997-2006). Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 55: 2106-2117. [ Links ]

Nishida, S. 1985. Taxonomy and distribution of the family Oithonidae (Copepoda, Cyclopoida) in the Pacific and Indian Oceans. Bull. Ocean Res. Inst. U. Tokyo., 20: 1-167. [ Links ]

Pasternak, A. F. and S. B. Schnack-Schiel. 2001. Feeding patterns of dominant Antarctic copepods: an interplay of diapause, selectivity, and availability of food. Hydrobiol., 453(1): 25-36. [ Links ]

Pasternak, A. F . and S. B. Schnack-Schiel . 2007. Feeding of Ctenocalanus citer in the eastern Weddell Sea: low in summer and spring, high in autumn and winter. Polar Biol ., 30(4): 493-501. [ Links ]

Postel, L., H. Fock and W. Hagen. 2000. Biomass and abundance. 83 -192. In: Harris, R. P., P. H. Weibe, J. Lenz, H. R. Skjoldal and M. Huntley. ICES Zooplankton methodology manual. Academic Press, London, U.K. 684 p. [ Links ]

Razouls, S., C. Razouls and F. De Bovee. 2000. Biodiversity and Biogeography of Antartic copepods. Antarct. Sci., 12(3): 343-362. [ Links ]

Razouls C., F. de Bovée, J. Kouwenberg and N. Desreumaux . 2019. 2005-2018- Diversity and Geographic Distribution of Marine Planktonic Copepods. Sorbonne Université, CNRS. Available: Available: http://copepodes.obs-banyuls.fr/en 04/01/2019. [ Links ]

Rodríguez, F., M. Varela and M. Zapata. 2002a. Phytoplankton assemblages in the Gerlache and Bransfield Straits (Antarctic Peninsula) determined by light microscopy and CHEMTAX analysis of HPLC pigment data. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 49 (4): 723-747. [ Links ]

Rodríguez, J., F. Jiménez-Gómez, J. M. Blanco and F.L. Figueroa. 2002b. Physical gradients and spatial variability of the size structure and composition of phytoplankton in the Gerlache Strait (Antarctica). Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 49 (4): 693-706. [ Links ]

Ross, R. M., E. E. Hofmann and L. B. Quetin . (Eds.). 1996. Foundations for ecological research west of the Antarctic Peninsula. AGU Antarctic research series, vol. 70. American Geophysical Union, Washington, DC. 448 p. [ Links ]

Ross, R. M ., L. B. Quetin , D. G. Martinson , R. A. Iannuzzi , S. E. Stammerjohn and R. C. Smith . 2008. Palmer LTER: patterns of distribution of five dominant zooplankton species in the epipelagic zone west of the Antarctic Peninsula, 1993-2004. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 55: 2086-2105. [ Links ]

Ross, R. M ., L. B. Quetin , T. Newberger, C. T. Shaw, J. L. Jones, S. A. Oakes and K. J. Moore. 2014. Trends, cycles, interannual variability for three pelagic species west of the Antarctic Peninsula 1993-2008. Mar. Ecol. Prog. Ser ., 515: 11-32. [ Links ]

Sailley, S. F., H. W. Ducklow , H. V. Moeller, W. R. Fraser , O. M. Schofield , D. K. Steinberg , L. M. Garzio, and S. C. Doney . 2013. Carbon fluxes and pelagic ecosystem dynamics near two western Antarctic Peninsula Adélie penguin colonies: an inverse model approach. Mar. Ecol. Prog. Ser ., 492: 253-272. [ Links ]

Schnack-Schiel, S. B., D.N. Thomas, C. Haas, G.S. Dieckmann and R. Alheit. 2001. The occurrence of the copepods Stephos longipes (Calanoida) and Drescheriella glacialis (Harpacticoida) in summer sea ice in the Weddell Sea, Antarctica. Antarct Sci., 13(2): 150-157. [ Links ]

Silva, M. P, M. Favero, S. Copello and R. Bastida. 2001. Does access to high-quality pelagic prey increase the breeding success of kelp gulls Larus dominicanus in the Antarctic peninsula. Mar Ornithol., 28: 85-88. [ Links ]

Smith, R.C., H. M. Diersen and M. Vernet . 1996. Phytoplankton biomass and productivity in the western Antarctic Peninsula region. Foundations for Ecological Research West of the Antarctic Peninsula. Antarctic Research Series, 70: 333-356. [ Links ]

Smith, R. C., K. S. Baker and W. Vernet. 1998. Seasonal and interannual variability of phytoplankton biomass west of the Antarctic Peninsula. J. Mar. Sys., 17(1-4): 229-243. [ Links ]

Smith Jr., W. O. and D. M. Nelson. 1986. Importance of the iceedge phytoplankton production in the Southern Ocean. Bio Sci., 36(4): 251-257. [ Links ]

Smith Jr., W.O., M. E. M. Baumann, D. L. Wilson and L. Aletsee. 1987. Phytoplankton biomass and productivity in the marginal ice zone of the Fram Strait during summer 1984. J. Geophys. Res., 92: 6777-6786. [ Links ]

Stammerjohn, S. E., D.G. Martinson, R.C. Smith and R.A. Iannuzzi. 2008. Sea ice in the western Antarctic Peninsula region: spatiotemporal variability from ecological and climate change perspectives. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 55: 2041-2058. [ Links ]

Steinberg, D. K, D.G. Martinson and D.P. Costa. 2012. Two decades of pelagic ecology of the Western Antarctic Peninsula. Oceanography, 25: 56-67. [ Links ]

Steinberg, D. K ., K. E. Ruck, M. R. Gleiber, L. M. Garzio , J. S. Cope, K. S. Bernard, S. E. Stammerjohn , O. E. M. Schofield, L. B. Quetin and R. M. Ross . 2015. Long-term (1993-2013) changes in microzooplankton off the western Antarctic Peninsula. Deep-Sea Res. Part I Oceanogr. Res. Pap ., 101: 54-70. [ Links ]

Treguer, P and G. Jacques. 1992. Dynamics of nutrients and phytoplankton, and fluxes of carbon, nitrogen and silicon in the Antarctic Ocean. Polar Biol ., 12: 149 -162. [ Links ]

Varela, M., E. Fernandez and P. Serret. 2002. Size-fractionated phytoplankton biomass and primary production in the Gerlache and south Bransfield Straits (Antarctic Peninsula) in Austral summer 1995-1996. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 49 (4): 749 -768. [ Links ]

Vaughan, D., G. Marshall, W. Connolley, C. Parkinson, R. Mulvaney, D. Hodgson, J. C. King, C. J. Pudsey and J. Turner. 2003. Recent rapid regional climate warming on the Antarctic Peninsula. Clim. Chang., 60: 243-274. [ Links ]

Ward, P, S. Grant , M. Brandon, V. Siegel, V. Sushin, V. Loeb and H. Griffiths. 2004. Mesozooplankton community structure in the Scotia Sea during the CCAMLR 2000 survey: January-February 2000. Deep-Sea Res. Part II. Top. Stud. Oceanogr ., 51: 1351-1367. [ Links ]

Whitehouse, M. J. and R. R. Veit. 1994. Distribution and abundance of seabirds and fur seals near the Antarctic Peninsula during the austral winter, 1986. Polar biol ., 14(5): 325-330. [ Links ]

Zhou, M., W. Nordhausen, and M. E. Huntley. 1994. ADCP measurements of the distribution and abundance of euphausiids near the Antarctic Peninsula in winter. Deep-Sea Res. Part I Oceanogr. Res. Pap ., 41: 1425-1445. [ Links ]

Zhou, M ., P. P. Niiler and J. H. Hu. 2002. Surface currents in the Bransfield and Gerlache Straits, Antarctica. Deep-Sea Res. I., 49 : 267-280. [ Links ]

Zhou, M ., P. P. Niiler , Y. Zhu and R. D. Dorland. 2006. The western boundary current in the Bransfield Strait, Antarctica. Deep-Sea Res. Part I Oceanogr. Res. Pap ., 53(7): 1244-1252. [ Links ]

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Received: April 26, 2018; Accepted: January 24, 2019

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