Horizontal and vertical distribution of mesozooplankton species richness and composition down to 2,300 m in the southwest Atlantic Ocean

ECOLOGY

Horizontal and vertical distribution of mesozooplankton species richness and composition down to 2,300 m in the southwest Atlantic Ocean

Sérgio L.C. Bonecker^I; Adriana V. de AraujoI, ^*; Pedro F. de Carvalho^I; Cristina de O. Dias^I; Luiz F.L. Fernandes^II; Alvaro E. Migotto^III; Otto M.P. de Oliveira^IV

^IUniversidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Laboratório Integrado de Zooplâncton e Ictioplâncton, Prédio do CCS, Bloco A, Cidade Universitária, Ilha do Fundão, 21941-590 Rio de Janeiro, RJ, Brazil

^IIUniversidade Federal do Espírito Santo, Departamento de Oceanografia e Ecologia. Av. Fernando Ferrari 514, 29075-910 Vitória, ES, Brazil

^IIIUniversidade de São Paulo, Centro de Biologia Marinha. Rodovia Manoel Hypólito do Rego, km 131.5, Praia do Cabelo Gordo, 11600-000 São Sebastião, SP, Brazil

^IVUniversidade Federal do ABC, Centro de Ciências Naturais e Humanas. Rua São Paulo, Jardim Antares, 09606-070 São Bernardo do Campo, SP, Brazil

ABSTRACT

We describe the species richness, distribution and composition of mesozooplankton over the continental shelf and slope, and in the water masses in the Campos Basin, southwest Atlantic Ocean. We analyzed the mesozooplankton from two oceanographic cruises (rainy and dry seasons, 2009) with samples taken in five different water masses from the surface to 2,300 m depth. In the Subsurface Water (SS), in both sampling periods, more species were recorded over the slope (rainy: 100; dry: 128) than the continental shelf (rainy: 97; dry: 104). Over the slope, species richness decreased with increasing depth: the highest values were observed in the South Atlantic Central Water (SACW), and the lowest values in the North Atlantic Deep Water (NADW), in both sampling periods. We recorded 262 species in 10 groups (Hydrozoa, Siphonophora, Ctenophora, Branchiopoda, Copepoda, Euphausiacea, Decapoda, Chaetognatha, Appendicularia e Thaliacea), with 13 new occurrences for the southwest Atlantic. Copepoda was the group with the highest species richness, containing 138 species. In both periods, the samples from SS, SACW and Antarctic Intermediate Water (AAIW)/Upper Circumpolar Deep Water (UCDW) were clustered in different faunistic zones, based on species composition. This study confirmed that zooplankton richness in the southwest Atlantic Ocean is underestimated, and suggests that additional efforts must be directed toward a better understanding of this fairly unknown region.

Key words: Deep sea; diversity; southeastern Brazil; zooplankton.

In pelagic marine environments, biodiversity is relatively low on the continental shelf, increases in oceanic waters and, in these areas, decreases with depth (ANGEL 1997, SMITH & BROWN 2002, LOPES et al. 2006). The pattern of increasing diversity from coastal to oceanic waters is attributed to continental influence, causing large fluctuations in temperature/salinity gradients and productivity, which favors dominance by relatively few species. The vertical pattern reflects the decrease in food availability due to light-limited primary production in deeper waters, and the decrease in temperature from the surface to the meso- and bathypelagic layers (RUTHERFORD et al. 1999). Therefore, few species are adapted to live in the pelagic realm of the deep ocean, which leads to lower species richness in these environments than in surface waters (SMITH & BROWN 2002).

The South Atlantic is one of the least known marine habitats, mainly with respect to some zooplankton groups (BOLTOVSKOY et al. 2003). Zooplankters play a key role in the control of phytoplankton production and are a critical food source for upper trophic levels, thus structuring pelagic ecosystems (LABAT et al. 2009).

Investigations on the epipelagic zooplankton off Brazil only began in the last century. BJÖRNBERG (1963) provided the first detailed account of epipelagic species communities, and BASSANI et al. (1999) reviewed the state of knowledge of planktonic biota between 21°S and 23°S. Between 1998 and 2000, surveys were carried out regarding zooplankton composition and distribution down to 200 m depth, between 12°S and 22°S (BONECKER 2006, BONECKER et al. 2007). Epipelagic studies in neighbouring regions were carried out by RAMIREZ & SABATINI 2000, ESKINAZI-SANT'ANNA & BJÖNBERG 2006, and LOPES et al. 2006. Information on the mesopelagic and bathypelagic community is nonexistent except for copepods (DIAS et al. 2010).

The Campos Basin is located on the central Brazilian coast. This region is characterized by the presence of different water masses, whose physical and chemical properties (e.g., temperature, salinity and dissolved oxygen) provide different potential habitats for many species in the pelagic realm. Due to coastal upwelling, the southern area of the Campos Basin has been the focus of most studies, mainly on circulation, nutrients, microplankton and epipelagic mesoplankton (VALENTIN 1984, VALENTIN et al. 1987). In this region, as throughout the southwest Atlantic, the vertical biodiversity pattern and the composition of mesopelagic is poorly known. Knowledge of bathyplankton is very scarce everywhere in the ocean.

In order to fill the gaps in knowledge of the species richness, distribution and composition of the mesozooplankton in deep waters in the southwest Atlantic, we describe the mesozooplankton composition from the surface to 2,300 m depth in the Campos Basin. We aimed to answer three questions: 1) Is there a horizontal gradient of mesozooplankton species richness between the continental shelf and the slope? 2) Is there a vertical gradient of mesozooplankton species richness? 3) Does each water mass, which has its own environmental characteristics, have a particular mesozooplankton species composition?

MATERIAL AND METHODS

The Campos Basin is located between 24°S and 20.5°S on the central Brazilian coast (Fig. 1). The climate is warm and humid, with a rainy season from November to February and a dry season from June to August (LACERDA et al. 2004). The continental shelf has a mean width of 100 km and the slope extends over a width of 40 km, with a 2.5° mean gradient (VIANA et al. 1998).

The Brazilian coast is influenced by the Brazil Current, a warm and oligotrophic western boundary current. It flows from the northeast toward the southwest, as part of the South Atlantic western boundary current system (STRAMMA et al. 1990). The water-column structure and distributions of the different water masses over the continental shelf and slope of the Campos Basin are the main factors that characterize the environment, and are determined mainly by temperature and salinity (MÉMERY et al. 2000, SILVEIRA & SCHMIDT 2000; Fig. 2). In the upper layers of the water column, the nutrient-poor Subsurface Water (SS) and the South Atlantic Central Water (SACW) are found. At deeper levels are the cold waters of the Antarctic Intermediate Water (AAIW), Upper Circumpolar Deep Water (UCDW), and North Atlantic Deep Water (NADW) (MÉMERY et al. 2000; Fig. 2).

Mesozooplankton (size >200 µm) samples were collected in two oceanographic cruises in 2009: February 25 to April 13 (rainy season) and August 5 to September 17 (dry season). The stations were distributed along six transects perpendicular to the coast organized in the South-North direction (A, C, D, F, H, and I). Each transect contained eight sampling stations, from the 25- to 3,000-m isobaths (25, 50, 75, 150, 400, 1,000, 1,900 and 3,000 m), four on the continental shelf and four on the slope (Fig. 1). Over the continental shelf, only Subsurface Water (SS) was collected; over the slope, samples were collected from the SS and from the other water masses, in the isobaths where they were present (Table I).

Mesozooplankton samples were collected during the night by horizontal hauls in the water-mass nuclei: Subsurface Water (SS), South Atlantic Central Water (SACW), Antarctic Intermediate Water (AAIW), and Upper Circumpolar Deep Water (UCDW; Table I). In the North Atlantic Deep Water (NADW), samples were collected by vertical hauls from the nucleus of this water mass (2,300 m) up to the limit of influence of the subjacent water mass (1,800 m), because of logistical problems associated with the speed of water currents (Table I). Hauls were made using a MultiNet® type midi (Hydro-Bios, 200 µm white mesh, 50 x 50 opening of frame), with digital flow meters attached to the inner net mouth and also an external meter to assess the filtration efficiency. Different set of nets were used at each depth, to prevent sample contamination. To determine the collecting depth, the MultiNet contained a depth sensor. Both the depth and water volume were transmitted to a computer simultaneously with the hauls. The horizontal hauls were made at a speed of 2 knots, during 10 minutes or until the filtered water volume reached 50 m³. Immediately after sampling, organisms were preserved in 4% buffered formalin. The mesozooplankton samples were obtained as part of the Habitats Project - Campos Basin Environmental Heterogeneity by CENPES/PETROBRAS.

In the laboratory, samples were divided into fractions using a Folsom Plankton Splitter (Hydro-Bios; MCEWEN et al. 1957) and at least 100 individuals per taxonomic group were sorted (FRONTIER 1981). The mesozooplankton taxonomic groups in this subsample were identified to species under a stereoscopic microscope and optical microscope.

All the specimens collected were deposited in the collection of the Integrated Zooplankton and Ichthyoplankton Laboratory of the Federal University of Rio de Janeiro (DZUFRJ 2007-2277, DZUFRJ 3075-4178, DZUFRJ 6726-8487, DZUFRJ 12622-16893).

We tested whether the mesozooplankton species richness varied depending on the region (continental shelf and slope) in the rainy and dry seasons, using non-parametric Mann-Whitney U test. To test differences in mesozooplankton species richness among water masses present over the slope, in both sampling periods, we used the non-parametric Kruskal-Wallis test.

We used hierarchical agglomerative cluster analyses (Q-mode) based on species composition to partition the samples into discrete groups in the rainy (69 species x 105 sampling stations) and dry seasons (69 species x 94 sampling stations). For this analysis, we used the Sørensen-Dice coefficient with average linkage method. The species composition was defined as the presence or absence of each species in each sample, and only species showing occurrence frequencies above 15% in each study period (rainy and dry seasons) were used in the analysis.

To identify the species that contributed most to the similarities and dissimilarities of the sample groups previously identified in the cluster analysis, we used the SIMPER (similarity of percentages) test. The analyses were performed using the statistical package Primer 6 (Primer-E Ltd., Luton, United Kingdom).

RESULTS

In the SS, we found more species over the slope (rainy season: 100 species, dry season: 128 species) than over the continental shelf (rainy season: 97 species, dry season: 104 species; Fig. 3) in the dry season (p < 0.05). On the slope, the species richness decreased with increasing depth. During the two sampling periods, we observed the highest values of species richness in the SACW (rainy season: 154 species, dry season: 141 species), and the lowest values in the NADW (rainy season: 39 species, dry season: 72 species; Fig. 3). In the rainy season, the mesozooplankton species richness showed significant differences in the NADW in relation to the other water masses, with the exception of IAW. In the dry season, the SS was significantly different from the other water masses (p < 0.05).

We recorded 262 species belonging to 10 zooplankton groups from 0-2,300 m depths (Table II). Copepoda was the group with the highest richness (138 species), followed by Siphonophorae (34), Euphausiacea (22), Hydrozoa (18), Chaetognatha (16), Appendicularia (14), Thaliacea (10), Decapoda (4), Branchiopoda (5) and Ctenophora (1). We found 13 new records for the southwest Atlantic Ocean: 10 Copepoda species, 1 Hydrozoa species and 2 Siphonophorae species. Among the new records, except for Lychnagalma utricularia (Siphonophorae) and Laodicea indica (Hydrozoa), which occurred in the SS, all of the other species were observed in the SACW, AAIW and/or the UCDW (Table II).

Hydrozoa. Aglaura hemistoma was the most frequent hydrozoan species (>70% in both sampling periods), followed by Liriope tetraphylla (>50% in both periods). The highest frequency of these species was recorded on the slope in the dry season and on the continental shelf in the rainy season, respectively. The SS (5 species) showed the highest number of species with exclusive occurrence in one water mass (Table II).

Siphonophorae. The most frequent siphonophore species was Diphyes bojani (>50% in both sampling periods). Abylopsis eschscholtzi was the second most frequent species (>79% in the rainy season and 81% on the slope during the dry season). Muggiaea kochi was the most frequent species (100% frequency) on the continental shelf in the dry season. The SACW (8 species) and SS (5 species) contained the most species with exclusive occurrence in one water mass (Table II).

Ctenophora. Two ctenophore species were recorded in the study period. Beroe sp. occurred only in the AAIW, and Hormiphora plumosa in the SACW (Table II).

Branchiopoda. Pseudevadne tergestina was the most frequent branchiopod species, and peaked in frequency on the continental shelf during the dry season. Penilia avirostris was the second most frequent species and was most frequent on the continental shelf, during the dry season. Only Pleopis schmackeri was recorded exclusively in the SS (Table II).

Copepoda. Clausocalanus furcatus was the most frequent copepod species (>90%) in both sampling periods. Temora stylifera was the second most frequent species (>80% in both periods), with a peak frequency on the continental shelf in the rainy season. The SACW contained the most species exclusive to that water mass (19), followed by the AAIW (10 species, Table II).

Euphausiacea. Euphausia americana was the most frequent euphausiacean species, with a peak frequency on the slope, in both sampling periods (>70%). Stylocheiron carinatum was the second most frequent species (>20% in both periods), with a peak frequency in the dry season, on the slope. In the SACW, we observed the highest number of species that occurred exclusively in one water mass (3 species; Table II).

Decapoda. Decapods occurred only in the SS and SACW, mostly in the rainy season. Only Stenopus hispidus occurred on both the continental shelf and the slope. Leander tenuicornis and Periclimenes longicaudatus were recorded only on the continental shelf, in the rainy season (Table II).

Chaetognatha. Flaccisagitta enflata was the most frequent chaetognath species, and occurred at all sampling stations throughout the study period. Parasagitta friderici was the second most frequent species. This species was found at all stations during the dry season and at 90% of the stations during the rainy season (Table II).

Appendicularia. The most frequent appendicularian species was Oikopleura longicauda, which occurred at all stations throughout the study period. The second most frequent species was Oikopleura fusiformis, which peaked in frequency on the slope during the dry season. The SACW contained the most species that occurred in only one water mass (2 species; Table II).

Thaliacea. Doliolum nationalis was the most frequent thaliacean, observed at all sampling stations throughout the study period. Thalia democratica was the second most frequent species and showed a frequency peak on the slope in the dry season. Five species occurred exclusively in the SS (Table II).

Cluster analysis indicated the formation of groups at a 55% similarity level during the rainy season (Fig. 4) and at a 40% similarity level during the dry season (Fig. 5).

During the rainy season, the arrangement of these groups indicated three faunistic areas: A) comprising mainly the samples from the SS; B) comprising the samples from the SACW, AAIW and UCDW, mainly; and C) comprising the samples of SACW, in the south and north regions of the study area (Fig. 4). The other samples were not associated with any of the large groups (over ten samples; Fig. 4). Among the species that contributed most to the similarity within the faunistic areas in the rainy season, Oncaea venusta (Copepoda), Oikopleura longicauda (Appendicularia), Parasagitta friderici, Flaccisagitta enflata (Chaetognatha), Doliolum nationalis (Doliolidae) and Diphyes bojani (Siphonophorae) contributed to the similarity of all groups, while other species contributed to the formation of only one faunistic zone (Table III).

During the dry season, the arrangement of the groups indicated three faunistic areas: A) comprising the samples of SS; B) comprising the samples of SACW, mainly; and C) comprising the samples of AAIW and UCDW (Fig. 5). The other stations were not associated with any of the large groups (over ten samples; Fig. 5). Some species contributed to the similarity of only one faunistic area, while Parasagitta friderici, F. enflata, O. venusta and O. longicauda contributed to the similarity of all groups (Table III).

Some of the rare species (occurrence frequency below 15% in the study period) were recorded in only one faunistic zone. The SS showed 29 exclusive species, e.g., Cunina frugifera, Sulculeolaria turgida, Hippopodius hippopus, Pleopis polyphemoides, Centropages violaceus, Calanopia americana and Pontellina plumata (Table II). In SACW, 34 species were exclusive to this faunistic zone, e.g., Enneagonum hyalinum, Lensia achilles, Gaetanus pileatus, Candacia tenuimana, Lophothrix quadrispinosa, Nematobrachion flexipes and Stylocheiron elongatum (Table II). In the AAIW/UCDW faunistic zone, 28 species showed exclusive records, e.g., Lensia havock, Gaetanus kruppi, Euaugaptilus facilis, Lophothrix latipes, Scaphocalanus brevicornis, Scaphocalanus elongatus, and Caecosagitta macrocephala (Table II).

DISCUSSION

The species richness and the composition of the zooplankton were primarily associated with the water masses present in the region. In the southwest Atlantic, as in most plankton studies elsewhere, the plankton fauna has mainly been surveyed in the upper layers (0-200 m; BJÖRNBERG 1963, BASSANI et al. 1999, RAMÍREZ & SABATINI 2000, BONECKER 2006, ESKINAZI-SANT'ANNA & BJÖRNBERG 2006, LOPES et al. 2006), and the mesopelagic is better studied but about the bathypelagic we know very little (DIAS et al. 2010). This study showed that the increase in depth is correlated with a decrease in the number of zooplankton species. In general, a decrease in diversity is expected with increasing depth (ANGEL 1997, ROBISON 2004). DIAS et al. (2010) observed a reduction in richness from the first few meters of the water column down to 2,300 m in the vertical distribution of copepods in the Campos Basin. In the present study, the highest species richness was observed in the first 250 m in the SACW, decreasing down to 2,300 m depth in the NADW. According to SMITH & BROWN (2002), the rapid declines of temperature and productivity associated with the increasing depth are the primary causes of this pattern of diversity decrease from 200 m depth to the deep ocean.

In SS, the slope showed higher species richness than the continental shelf in the dry season. This trend to increasing diversity toward the oceanic region was discussed by Lopes et al. (2006), and has been observed in many studies comparing neritic and oceanic areas (e.g., RAKHESH et al. 2006, ZHANG et al. 2009). The tropical oceanic regions are oligotrophic (BOLTOVSKOY 1981) and low concentrations of nutrients are associated with more stable environments (ANGEL 1993). This characteristic result higher richness in ocean regions than in neritic areas (ANGEL 1993).

The most frequent species of each mesozooplankton group found on the continental shelf and slope of the Campos Basin have been observed along the Brazilian coast (e.g., GUSMÃO et al. 1997, LOPES et al. 1999, DIAS et al. 2010). We found 13 new records for the southwest Atlantic Ocean; until the present study, the distribution areas of these species in the Atlantic Ocean had been recognized only from the North Atlantic, central South Atlantic and/or southeast Atlantic (BOUILLON 1999, SUÁREZ & GASCA 1989, GASCA 2002, RAZOULS et al. 2000, 2013; Table IV).

In both sampling periods, the samples from SS, SACW and AAIW/UCDW were clustered in different faunistic zones. The species compositions of the AAIW and UCDW were not distinct, probably due to their similar circulation patterns (REID 1989), salinity and temperature (REID 1989, MÉMERY et al. 2000; Fig. 2). Some rare species (occurrence frequency below 15%) showed a bathymetric distribution restricted to a single faunistic zone (SS, SACW and AAIW/UCDW). The vertical distributions previously recorded for most of these species concords with the results of this study (BRADFORD-GRIEVE et al. 1999, BOUILLON 1999, CASANOVA 1999, GIBBONS et al. 1999, PUGH 1999).

Understanding the distribution patterns of species or higher taxa is more complicated than understanding the patterns of density and biomass, since species do not react uniformly to a given environment. Water-mass characteristics and smaller-scale oceanographic features affect the habitat and bathymetric distribution of these species (FERNÁNDEZ-ÁLAMO & FÄRBER-LORDA 2006). The occurrence of epipelagic species (e.g., Clausocalanus furcatus and Penilia avirostris) in the meso-bathypelagic zones can be attributed to: 1) contamination, 2) sampling of dead individuals, or 3) increase in their depth distribution. The hypothesis of contamination is unlikely because the sampling was done with a multinet, which has a robust opening-closing mechanism and is suitable for stratified depth samples (SAMEOTO et al. 2000). In addition, different set nets were used at each depth. Another possibility is that specimens of epipelagic species recorded in deep water masses were dead individuals in the process of settling. This hypothesis cannot be ruled out, since we did not use any technique, such as neutral red stain for crustaceans, which could distinguish dead from living individuals (MARCUS et al. 2004, TANG et al. 2006, JESSOPP 2007). Otherwise, the extension of the depth distribution is possible, in view of the lack of studies in deep habitats in the southwest Atlantic Ocean.

Some species that contributed to the delimitation of all groups, occurring from the surface to the deep water masses, were previously classified as epipelagic until this study, e.g., Parasagitta friderici (CASANOVA 1999, LIANG & VEGA-PÉREZ 2001), while the other species had been recorded from the deep ocean, e.g., Oncaea venusta, Flaccisagitta enflata, and Doliolum nationalis (OZAWA et al. 2007, WEIKERT & GODEAUX 2008, DIAS et al. 2010). In the SS, during both study periods, Corycaeus giesbrechti and Liriope tetraphylla contributed to the delimitation of this group. These species are characteristic of the epipelagic region (LOPES et al. 1999, BUECHER & GIBBONS 2000, BENOVIC et al. 2005), although C. giesbrechti has been recorded in the upper 500 m of the Sargasso Sea off Bermuda (DEEVEY 1971), and down to 1,000 m in the Campos Basin (DIAS et al. 2010). In the SACW, Decipisagitta sibogae and Krohnitta subtilis contributed to the delimitation of this group in the two periods. These species were classified as mesopelagic by CASANOVA (1999). Decipisagitta sibogae has been recorded between 200-600 m in the Sargasso Sea (PIERROT-BULTS & NAIR 2010) and K. subtilis has been recorded at 600-800 m in the Pacific Ocean (OZAWA et al. 2007, PIERROT-BULTS & NAIR 2010) and at 400 m off the Chilean coast (ULLOA et al. 2000). All species that contributed most to the similarity of the group from deep water masses in both sampling periods are classified as mesopelagic or bathypelagic, except Dolioletta gegenbauri, Oikopleura fusiformis, and Rhincalanus cornutus, which are classified as epipelagic. Dolioletta gegenbauri is a common species off the Brazilian coast in areas under the influence of coastal and tropical water (LOPES et al. 2006). Oikopleura fusiformis is found in coastal and oceanic waters and is more frequent in the latter (BONECKER & CARVALHO 2006). Until this study, O. fusiformis had not been recorded in the mesopelagic and bathypelagic regions. Although it has been classified as epipelagic (BRADFORD-GRIEVE et al. 1999), R. cornutus was observed below 600 m off the coast of Florida, USA (MOORE & O'BERRY 1957), in the upper 500 m in the Sargasso Sea off Bermuda (DEEVEY 1971), and below 2,000 m in the Campos Basin (DIAS et al. 2010).

The sample grid and number of zooplankton groups included in this study are more extensive than any previous study in the southwest Atlantic Ocean, and helped to fill the gap in understanding mesozooplankton vertical distribution. The results of this study extended the vertical distribution of some zooplankton species previously classified as epi-mesopelagic species. We confirmed that zooplankton richness in the southwest Atlantic Ocean is currently underestimated, and we suggest that additional efforts must be directed toward a better understanding of this fairly unknown region.

ACKNOWLEDGMENTS

The authors thank the team of the Zooplankton and Ichthyoplankton Integrated Laboratory of Federal University of Rio de Janeiro, in particular Cláudio de S. Ressur and José R.S. Silva for sorting the samples. We also thank Janet W. Reid for improving the English text, and the following researchers for their help with identifications: Michele Arruda (Chaetognatha), Paulo R.F.C. Costa and Marta C.C. Quintas (Branchiopoda); Suzanna C. Vianna and Rafaela A. Nunes (Copepoda); Patrícia Alpino, Lohengrin Fernandes, Ralf Schawmborn, Cíntia Cardoso, and Ana Cecilia R. Resende (decapod larvae); and Andrea S. Freire (Euphausiacea). Finally, we thank Petrobras, which made possible the sampling and material analyses.

LITERATURE CITED

Submitted: 28.I.2014

Accepted: 16.VIII.2014

Editorial responsibility: Rosana M. da Rocha

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Publication Dates

• Publication in this collection
  04 Nov 2014
• Date of issue
  Oct 2014

History

• Received
  28 Jan 2014
• Accepted
  16 Aug 2014