Spring plankton communities in the southern Patagonian shelf: Hydrography, mesozooplankton patterns and trophic relationships

Journal of Marine Systems 94 (2012) 33–51

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Spring plankton communities in the southern Patagonian shelf: Hydrography, mesozooplankton patterns and trophic relationships M.E. Sabatini a, b, c,⁎, R. Akselman b, R. Reta b, d, R.M. Negri b, V.A. Lutz a, b, c, R.I. Silva b, V. Segura b, M.N. Gil a, e, N.H. Santinelli f, A.V. Sastre f, M.C. Daponte g, J.C. Antacli a, b, c a

Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Rivadavia 1917, C1033AAJ Buenos Aires, Argentina Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo N° 1, B7602HSA Mar del Plata, Argentina Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET-Universidad Nacional de Mar del Plata, Argentina d Universidad Nacional de Mar del Plata, Funes 3350, B7602AYL Mar del Plata, Argentina e Centro Nacional Patagónico (CENPAT, CONICET), Bvd. Brown 2915, U9120ACD Puerto Madryn, Argentina f Universidad Nacional de la Patagonia San Juan Bosco, Roca 115, U9100AQC Trelew, Chubut, Argentina g Universidad de Buenos Aires, Pab. II, Ciudad Universitaria, 4° piso, lab. 33, C1428EHA Buenos Aires, Argentina b c

a r t i c l e

i n f o

Article history: Received 25 February 2011 Received in revised form 5 October 2011 Accepted 7 October 2011 Available online 20 October 2011 Keywords: Southern Patagonian shelf Plankton Community structure Trophic relationships Hydrography

a b s t r a c t A strong interest in the southern Patagonian shelf has emerged in recent years, along with the increasing recognition of its high biological productivity. Knowledge of the pelagic food web structure that supports the richness of this system is still developing, but there are indications that mesozooplankton occupy a pivotal position, as consumers of smaller plankton and as vital prey for fish and squid. All plankton communities in the size 2 μm–20 mm, total and size-fractioned chlorophyll a (Chl a), nutrients and hydrology were surveyed simultaneously in October 2005 between 47°S–55°S. Picoplankton, nanoplankton and microplankton were taxonomically and functionally (autotrophs, heterotrophs) sorted within each size fraction. Plankton data and trophic relationships were examined through multivariate statistics. At that time fairly homogeneous thermal conditions prevailed over most of the shelf but weak saline horizontal gradients were evident. N/P ratios indicated no N or P limitation for phytoplankton. Surface concentrations of total Chl a were particularly high in the Grande Bay area at ca. 51°S near shore (28.6 mg m − 3) and at ca. 47°S on the shelfbreak (7.7 mg m− 3). At both locations the contribution of the Chl a > 5 μm fraction was remarkably high. The dinoflagellate Prorocentrum minimum (10 · 10 6 cells L− 1) and the diatom Thalassiosira cf. oceanica (1.3 · 10 6 cells L− 1) were respectively blooming at these sites. Otherwise b 10 μm plankton prevailed overall. Copepods largely dominated the >200 μm fraction. Three mesozooplankton assemblages typical of the inner, middle, and outer shelf were identified. The inner and middle shelf assemblages overlapped slightly but were spatially separated from the outer shelf community. Adults and late copepodids of Drepanopus forcipatus were typical of the inner shelf assemblage. Middle-shelf species included the copepod Ctenocalanus vanus, the amphipod Themisto gaudichaudii and the chaetognath Sagitta tasmanica, while an assortment of taxa characterized the outer sector. Latitudinal patterns in mesozooplankton community composition were less noticeable than cross-shelf patterns. No clear distribution of phytoplankton and protozooplankton assemblages was apparent when the whole b 200 μm plankton community structure was considered. In contrast, communities in the optimal size food for copepods (> 10–200 μm) were slightly different across shelf. Overall, spatial patterns of mesozooplankton and food availability matched weakly, suggesting a poor coupling between consumers and their prey communities at the time. Significant correlations were found particularly with large autotrophs and heterotrophs. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The southern Patagonian shelf identifies the wide, flat continental shelf extending off southern Argentina from ca. 47° to 55°S (Fig. 1). ⁎ Corresponding author at: Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo No 1, B7602HSA Mar del Plata, Argentina. Tel.: + 54 223 486 2586/1292, 266(local); fax: + 54 223 486 1830. E-mail address: [email protected] (M.E. Sabatini). 0924-7963/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2011.10.007

This is one of the world's most productive and complex marine ecosystems, including a variety of commercially important fisheries (Sánchez and Bezzi, 2004) and large marine mammal (Bastida and Rodríguez, 2003) and seabird populations (Croxall and Wood, 2002; Yorio et al., 1999). Knowledge of the pelagic food web structure that supports the richness of this system is still developing, but there are indications that zooplankton occupy a pivotal position, as consumers of smaller plankton and as vital prey for fish and squid (Antacli et al., 2011;

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M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

South America S

San Jorge Gulf

Study Area

47°

PD

50 m

Pto. Deseado

49 48 47 46 100 m

45

44

39 38 43 42 41 40

1000 m

49°

SFP

S. F. Paula 52

51

200 m

50

GB 75

747372

71

70

69

Malvinas Is.

68

Grande Bay Magallanes St 53

. MAG 54

55

56 57

53°

BUR

aire

St.

Tierra del Fuego

58

59

68°

66°

60

61

62

Burdwood Bank

1000 m

Le M

W

51°

200 m

64°

62°

55°

60°

58°

Fig. 1. Southern Patagonian shelf. Location of the study area and sampling transects (PD, Puerto Deseado; SFP, San Francisco de Paula; GB, Grande Bay; MAG, Magallanes; BUR, Burdwood).

Ivanovic and Brunetti, 1994; Ramírez, 1976; Sánchez, 1999). The overall food web of the southern Patagonian shelf ecosystem has been described from isotopic analysis as triangular, with marine mammals and birds at the apex, and zooplankton forming a broad step close to the basis. At intermediate levels, zooplanktivorous taxa are highly dominant in terms of both number of species and biomass, further highlighting the importance of zooplankton for the ecosystem productivity (Ciancio et al., 2008). A strong interest in the southern Patagonian shelf has emerged in recent years, along with the increasing recognition of its high biological productivity. Biomasses of primary producers appear to be locally enhanced in the Grande Bay area (Fig. 1) throughout spring–summer (Lutz et al., 2010; Rivas et al., 2006; Romero et al., 2006) and large mesozooplankton biomasses are recurrently recorded by the end of the productive season (Sabatini and Álvarez Colombo, 2001; Sabatini et al., 2004). Ciliate density and biomass are in turn low, likely because of predation control by mesozooplankton (Santoferrara and Alder, 2009). Respiration of zooplankton and the increase of CO2 by convection in these hotspots would result in a large seasonal source of CO2 to the atmosphere (Bianchi et al., 2005). In contrast, by late summer/fall the gross primary production seems to exceed respiration of the small plankton community of b500 μm over most of the shelf off Argentina, suggesting a low heterotrophic activity within the smaller size fraction (Schloss et al., 2007). Understanding the role of mesozooplankton in the fate of biogenic carbon is, therefore, particularly important in this region, all the more on account that the Patagonian shelf as a whole (i.e., ~ 38°S to ~ 55°S) is considered

one of the strongest CO2 sinks per unit area in the world ocean for most of the year (Bianchi et al., 2009). The southern Patagonian shelf is a composite area with a unique combination of characteristics. The prevalent westerly winds, high tidal amplitudes, large freshwater inflows, the strong influence of the bordering Malvinas Current, and the presence of three typical water masses (primary defined by salinity, Bianchi et al., 1982) generate a complex circulation pattern and cross-shelf exchanges (Matano et al., 2010; Palma et al., 2008), along with a multiplicity of fronts: tidal mixing, estuarine and river plume, water mass convergence, and a shelf-break front (Acha et al., 2004; Belkin et al., 2009; Sabatini et al., 2004). This hydrographic diversity would translate into habitat heterogeneity for plankton communities in terms of either nutrient or prey availability, eventually promoting dissimilar food web structures (Kiørboe, 1993). Habitat complexity and heterogeneity have been linked to changes in organism abundance and diversity in a variety of aquatic settings (e.g., Bakun, 2006; Levin and Dayton, 2009). In the oceans, water interfaces and hydrographic discontinuities are major structuring agents of ecological assemblages, which probably generate cascading effects on the patterns of diversity and productivity. The present study reports the results of the first out of three seasonal multidisciplinary surveys conducted over the southern Patagonian shelf during spring, summer and late winter in 2005–2006. These surveys offered the exceptional opportunity of expanding the temporal window for environmental studies in the study area, which until now had been mostly restricted to summer/fall. Hence,

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

this is the first combined physical–chemical–plankton data set ever collected for the southern Patagonian shelf in springtime. The aim of this paper was to investigate the spatial patterns of mesozooplankton during the austral spring in relation to the hydrography and structure of the overall plankton community. Here we hypothesized that the spatial environmental heterogeneity (biotic and abiotic) of the southern Patagonian shelf would drive distinct zooplankton assemblages, by influencing both composition and productivity. We assumed that the differential establishment of the seasonal thermal stratification along the shelf during the spring would further enhance habitat differences for mesozooplankton. 2. Materials and methods 2.1. Sampling The study area extended over the continental shelf off Argentina in the SW Atlantic Ocean from ca. 47° to 55°S. Data were collected in early spring (October 2005) on a cruise with the R/V ARA “Puerto Deseado”. Sampling was conducted along five transects covering different hydrological areas across the shelf: (i) off Puerto Deseado (PD) at ca. 47°S, (ii) off San Francisco de Paula (SFP) at ca. 50°S, (iii) in middle Grande Bay (GB) at 51°S, (iv) off Magallanes (=Magellan) Strait (MAG) at ca. 53°S, and (v) off Tierra del Fuego approaching the Burdwood Bank (BUR) at ca. 54°S (Fig. 1). At all stations continuous profiles of temperature, salinity and fluorimetry were recorded with a Sea-Bird 911 CTD, and a Sea-Point fluorometer mounted onto the CTD. Niskin bottles were used to collect samples for the analysis of nutrients, chlorophyll a (total and b5 μm), and for the study of pico-, nano- and microplankton sizefractions. Three depths were sampled according to the fluorometric profile (surface with a bucket, at fluorescence maximum and at a selected depth within the stratum below) with Niskin bottles (Table 1). Samples for total chlorophyll a (Chl a) determination were filtered through glass-fiber filters (Millipore APFF, similar to Whatman GF/ F); replicate samples were pre-filtered through 5 μm pore polycarbonate filters to determine the Chl a concentration in the fraction b5 μm size. Filters were immediately frozen in liquid nitrogen (−196 °C) and kept in ultrafreezer (−86 °C) until analysis once at the laboratory. Water samples for the measurement of nitrate, phosphate and silicate were preserved at − 20 °C. Samples for the study of pico and nanoplankton were preserved with formaldehyde 0.3%; 500 ml were then filtered through black polycarbonate membranes (0.2 μm) and kept at −20 °C for analysis by epifluorescence microscopy; another subsample was kept at 4 °C for analysis with inverted microscope. Samples for quantitative analysis of microplankton were preserved with Lugol solution, and qualitative samples were additionally collected with a Hensen net (25 μm) and fixed with formaldehyde. Zooplankton was sampled with a Motoda net 60 cm mouth diameter and 200 μm mesh size mounted on a frame provided with a closing mechanism (Motoda, 1969). Tows were performed obliquely within two strata below and above the depth of maximum fluorescence (or selected depths when the water column was homogeneous) (Table 1). Filtered volumes were estimated by a digital flowmeter mounted on the sampler. Samples were preserved with formaldehyde 5%. We are aware that larger and faster-swimming zooplankton such as euphausiids, amphipods and chaetognats were likely undersampled by the Motoda net because this is a slow-type sampler. Their signal was nevertheless in the samples, and this was assumed to be proportional to their actual abundance. Most collections were made at daylight hours (=15 stations vs. 8 stations at nighttime, Table 1) because sampling time relied on the arrival at stations after the cruise general track. This circumstance most likely introduced some bias in the estimation of zooplankton abundances. Depending on species or groups, during daytime some animals may

35

have been deeper than sampled in the water column due to diel vertical migration behavior. 2.2. Chemical and plankton analysis Chlorophyll a concentrations were measured by a modification of the fluorometric method (Holm-Hansen et al., 1965). Pigments on filters were extracted in 100% methanol and fluorescence was read in a Perkin Elmer LS3 spectrofluorometer (for further details see Lutz et al., 2010). Nitrate, nitrite, phosphate and silicate concentrations were measured at CENPAT using an automatic nutrient analyzer (Skalar). The N/P ratio was determined as (NO3 + NO2)/PO4. Pico and smaller nanoplankton countings were carried out with epifluorescence microscopy and image analysis according to their Chl a and phycobilin contents (Verity and Sieracki, 1993), while those of larger nanoplankton and microplankton were performed with an inverted microscope provided with a coupled imaging system (Lund et al., 1958). Mesozooplankton sub-samples were enumerated under a stereoscopic microscope (LEICA S8 APO). At least 200 adult or C4–5 copepods were classified to species and all other zooplankton taxa occurring in the sub-sample were enumerated. Normally a total of 700–1000 individuals were counted for each sample. Taxonomic identification was primarily based on Ramírez (1970a,b, 1971, 1973) and Boltovskoy (1981, 1999). Copepods were staged and sexed after Bradford et al. (1988), Heron and Bowman (1971) and Hulzemann (1991). All development stages of chaetognaths were sorted out and identified to species level according to Casanova (1999). 2.3. Data analysis/statistical methods The extension of either mixed or stratified areas over the shelf was examined through the well known Simpson (1981) stability parameter. It was derived from vertical profiles of density at 1 m depth intervals. The assessment of the relative contribution of freshwater to the stratification of the water column was additionally estimated by a modification to Simpson's equation (after Gowen et al., 1995): Φs ¼ g h−h ∫

0

  ′ ′ ρ −ρ 0 z dz;

where ρ′ is the density at depth z calculated using observed salinity and the mean temperature of the water column. The definition of mixed layer depth is a subjective matter with numerous criteria commonly in use (e.g., de Boyer Montégut et al., 2004 and references therein). In this study mixed layer depths were determined using a density threshold difference of 0.01 kg m − 3 relative to near surface values, after testing best fitting with in situ profiles (Reta, 2009). The mixed layer depth (MLD) was thus estimated using a conventional threshold method as: Δσ θ ¼ σ θ surface−σ θ z > 0:01 kg m

−3

ðthresholdÞ

where σθ is potential density; as for the surface layer, we considered a mean value over the upper 5 m to minimize noise mainly due to the CTD entering into the water. Plankton community data were examined through multivariate statistics using the PRIMER software package (Clarke and Warwick, 1994) version 5.2.9 (Primer-E). Picoplankton, nanoplankton and microplankton cell counts (cells l − 1) were taxonomically (e.g., diatoms, dinoflagellates, ciliates, flagellates, etc.) and functionally (autotrophs, heterotrophs) grouped by size fractions (2–5 μm, >5–10 μm, >10– 20 μm, >20–200 μm); smallest b2 μm autotrophs were also included in the analysis but bacteria were not. Only surface data were

36

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

Table 1 Sampling overview of cruise R/V ARA “Puerto Deseado” (October 2005). Stations, sampled parameters (biotic and abiotic), sampling dates, times and depths. (MDA, Motoda sampler). ST

Transect

Date

Local time

Bottles depth

Total Chla

Size-fractioned Chla

Nutrients

Plankton b 10 μm

38

PD

10/16/05

21:18

X X X

X

PD

10/17/05

00:40

X X X X

X X X

39

40

PD

10/17/05

04:12

41

PD

10/17/05

07:30

42

PD

10/17/05

10:16

43

PD

10/17/05

13:42

44

PD

10/17/05

17:14

45

PD

10/17/05

20:12

0 40 100 0 35 100 0 20 40 0 25 100 0 30 75 0 20 90 0 100 0 25 80 0 30 70 0 20 50 0 10 30 0 10 30 0 10 70 0 20 70 0 10 35 0 10 50 0 15 50 0 15 70 0 15 50 0 15 50 0 15 50 0 10 70 0 50 215 0 50 115 0 10 50

46

PD

10/17/05

23:48

47

PD

10/18/05

02:20

48

PD

10/18/05

05:41

49

PD

10/18/05

08:34

50

SFP

10/19/05

08:26

51

SFP

10/19/05

11:26

52

SFP

10/19/05

14:42

53

MAG

10/20/05

06:27

54

MAG

10/20/05

10:47

55

MAG

10/20/05

14:36

56

MAG

10/20/05

17:53

57

MAG

10/20/05

21:47

58

BUR

10/21/05

08:46

59

BUR

10/21/05

12:44

60

BUR

10/21/05

16:33

61

BUR

10/21/05

20:30

62

BUR

10/21/05

23:58

X

X X X X X X X X X X

X

X X X X X X X X X

X X X X X X X X X

X

X

X

X

Plankton > 10 μm

X X X X X X X X X X X X X X X X X

Zooplankton > 200 μm

Strata depth (MDA)

X X

0–15 50–15

X X

0–15 35–15

X X

0–15 50–15

X X

0–15 40–15

X X

0–10 35–10

X X

0–10 30–10

X X

0–20 40–20

X X

0–20 30–20

X X

0–15 25–15

X X

0–10 40–10

X X

0–15 40–15

X X

0–20 60–20

X X

0–20 60–20

X X

0–30 60–30

X X

0–20 40–20

X X

0–20 60–20

X failed

0–20

X

X X X X X X X

X X X X X X

X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X

X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X

X X X X X X

X

X

X

X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X

X

X

X

X

X X

X

X

X

X X

X

X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X X

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

37

Table 1 (continued) ST

Transect

Date

Local time

Bottles depth

Total Chla

63 64 65

– – –

10/22/05 10/22/05 10/22/05

03:41 10:10 13:43

66 67 68

– – BG

10/22/05 10/22/05 10/23/05

17:20 21:40 00:36

69

BG

10/2305

03:35

70

BG

10/23/05

13:10

X X X X X X X X X X X X X X

71

BG

10/23/05

15:30

72

BG

10/23/05

18:48

Ad 73

BG BG

10/23/05 10/23/05

20:49 21:30

74

BG

10/23/05

22:28

75

BG

10/24/05

01:44

0 0 0 10 70 0 0 0 10 50 0 10 40 0 40 0 10 40 0 10 40 0 0 5 40 0 15 45 0 10 20

X X X X X X X X X X X X X X X

Size-fractioned Chla

Nutrients

Plankton b 10 μm

Plankton > 10 μm

Zooplankton > 200 μm

Strata depth (MDA)

X X X X X X X X X X X X X X

X X

0–20 40–20

X X

0–25 50–25

X X

0–20 50–20

X X

0–15 80–15

X X

0–15 40–15

X

0–20

X

X X X X X X

X X X X X X

X

X X X X X X

X X X X X X

X

X X X X X

X X X X X

considered for the statistical examination of the b200 μm communities in particular, because they comprised the most complete array of data matching simultaneous sampling of all plankton size fractions and abiotic variables. All taxa identified in the mesozooplankton samples were included in the analysis independently of their abundance, and ontogenetic stages of species/groups were maintained separately. In this way we wanted to see whether there were differences in terms of community development, since very often dissimilarities between zooplankton communities are due to species abundances rather than to species composition. In turn, species abundances may be largely determined by recruitment rates and timing (Ward et al., 2006). Mesozooplankton abundances at the two sampling depths (ind m -3) were standardized to individuals m − 2 through integration by the trapezoidal method, either within each of the two sampled strata or for the whole sampled column. At stations where mesozooplankton assemblages were contrasted against their potential food (>10–200 μm) within the water column, nano (10–20 μm) and microplankton cell counts obtained from samples at three depths were integrated into two layers equivalent to zooplankton sampling strata.. Prior to running PRIMER analysis, plankton abundances were in all cases double-root transformed to normalize the data and reduce the influence from very abundant species (e.g. Drepanopus forcipatus and blooming phytoplankton species). To compare the mesozooplankton community structure at different locations, a Bray–Curtis similarity matrix was calculated from the (double-root transformed) depth-integrated abundances of all identified taxa. This matrix was the basis for cluster analysis and non-metric multi-dimensional scaling (MDS), as well as for statistical analysis of similarity (ANOSIM) and species contribution (SIMPER). Cluster analysis (q-type and average linkage method) and MDS were applied to differentiate mesozooplankton communities over the shelf and to

X

X

X X X X X X X X X

assess their relationships, respectively. The significance of differences between zooplankton assemblages was evaluated by one-way ANOSIM, while the contribution of species/taxa to each group similarity/ dissimilarity was examined through the SIMPER routine. Typical species of each group, i.e., those that occurred at a consistent abundance at most locations, were recognized from relatively larger ratios between the species' contribution to the average similarity within a group (SIM) and the standard deviation (SD) of their contribution, SIM/SD (Clarke and Gorley, 2001). Environmental variables likely to be associated with the mesozooplankton multivariate patterns through the water column were analyzed by principal component analysis (PCA). Representative variables were selected a priori under the assumption that temperature, salinity, nutrient availability, stability and light (as day-light length) are key factors in shaping plankton communities, and thus in apportioning the study area into hydrological sub-areas. The influence of physico-chemical factors on the mesozooplankton assemblages was examined through the BIO-ENV routine (Clarke and Ainsworth, 1993). The Spearman rank correlation between Bray–Curtis similarity matrices of mesozooplankton and normalized Euclidean distances of the variables significantly correlated with the environmental principal components was thus examined; these variables were either averaged or calculated for the first 100 m water column. The influence of (size-fractioned) phytoplankton and protozooplankton assemblages on the mesozooplankton abundance and composition was tested through several RELATE tests. This test allows multivariate comparisons of two biological similarity matrices, as opposed to the BIO-ENV routine (Clarke and Gorley, 2001). RELATE tests were conducted to surface data only because, as mentioned earlier, these built-up the most complete set matching all size-fractions sampled simultaneously.

38

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

68°

70° 47°

66°

64°

62°

60°

58° 70°

68°

66°

64°

62°

60°

58°

B

A

10 9.5

47°

9 8.5 49°

49°

51°

51°

8 7.5 7 6.5

53°

6

53°

5.5 5 55°

55°

4.5 4

47°

C

D

34.5

47°

34.3 49°

34.1

49°

33.9 33.7

51°

51°

33.5 33.3 53°

53°

55°

55°

33.1 32.9

70°

68°

66°

64°

62°

60°

58° 70°

68°

66°

64°

62°

60°

32.7 32.5

58°

Fig. 2. Surface and bottom temperature and salinity fields over the southern Patagonian shelf during early spring (October 2005). A, surface temperature; B, bottom temperature; C, surface salinity; D, bottom salinity.

3. Results 3.1. Physico-chemical settings The temperature fields at the time of the cruise were relatively homogeneous both horizontally and vertically (on average 6.5 °C ± 1 °C), except for the area approaching the continental slope. Overall it decreased slightly from NW to SE (Fig. 2A and B). Thermoclines

S 47°

A

were not well established yet and only weak horizontal gradients were evident at the resolution of our in situ (CTD) data. Salinity increased from 32.5 in coastal waters to 34.1 and 34.3 near the slope, at surface and bottom respectively (Fig. 2C and D), in accordance with the occurrence of the three water masses which are typical in the study area (Fig. 3A and B). Distinct salinity waters create several surface fronts of different intensity over the shelf. The contrast between the Magellan Strait

S

B

47°

49°

49°

51°

51°

53°

53°

55°

55°

W 68°

66°

64°

62°

60°

58° 70°

68°

66°

64°

62°

60°

W

Fig. 3. Horizontal distribution of water masses at surface (A) and bottom (B) across sampling stations over the southern Patagonian shelf during the survey (October 2005). Magellan Strait Water (S b 33.4, ● orange), Subantartic Shelf Water (33.4 b S b 34.0, ∇ yellow) and Subantartic Water (S > 34.0, ♦ sky blue).

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

PD

SFP

MAG

BUR

39

GB

40 temperature salinity

Stability (Jm-3)

30

20

10

0 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 59 60 61 62 68 70 71 72 73 74 75

Station# Fig. 4. Relative contribution of temperature and salinity to stratification over the study area during early spring. Estimates from Simpson (1981) stability parameter Φ and adjusted equation to account for salinity input (after Gowen et al., 1995). Note as reference that critical values of Φ > 40–50 J m− 3 are commonly used to denote strongly stratified waters in summertime (Bianchi et al., 2005; Sabatini et al., 2000, 2004).

Waters (b33.4) with the Subantarctic shelf waters (b34.0) (Bianchi et al., 1982; sensu Palma et al., 2008) generates a front that extends parallel to shore along most of the study area, the Magellan salinity front. This has been previously referred to as a typical Mid-shelf water mass boundary front (Sabatini et al., 2004), also named Atlantic cold estuarine front (Acha et al., 2004). During the survey, its signal at surface was evident at ca. 100–200 km from shore and the gradients slightly decreased northwards, i.e., with increasing distance from the source of diluted waters from the Magallanes Strait [zonal gradient = 0.104 km − 1 at 53°S (MAG), 0.052 km − 1 at 51°S (GB) and 0.045 km − 1 at 47°S (PD)]. Other rather coastal horizontal gradients were detected at a variable distance from shore (20–30 km) depending on the section (zonal gradient = 0.043 km − 1 at 53°S, 0.073 km − 1 at 51°S and 0.051 km − 1 at 47°S). These are likely tidal estuarine–plume type fronts, as their origin seems to be related to freshwater discharges onto the shelf (Sabatini et al., 2004). The sharpest horizontal gradient of salinity (zonal gradient = 0.113 km − 1) during the cruise was recorded at ca. 54°S (BUR) and 80 km from shore. This is the southernmost signal of the Shelf-break front, which forms from the contrast of Subantarctic shelf waters (>33.4– 34.0) with cold and dense Subantarctic waters (>34.0). The signal at the other extreme of our surveying area (47°S, PD transect) was much weaker (zonal gradient = 0.039 km − 1) and located at 350–400 km offshore. The water column was not stratified either thermally or by salinity over most of the shelf except for the outer stations on PD and BUR transects, both under the influence of the colder and more saline waters of Malvinas Current. Comparatively with the surrounding shelf, nonetheless, the water column was slightly stratified in the GB area (Fig. 4). The mixed layer depth (MLD) was highly variable over the study area. Two different forcing mechanisms could be recognized: the weak surface heating by solar radiation to the north, and the entrance of low salinity waters into the region to the south. At coastal stations (St 48 and 49) on the PD transect the water column was completely homogeneous — likely due to strong tidal mixing, while in close proximity eastwards, a weak stratification in the surface layer produced an incipient thermocline and determined a MLD at 11 m. The same process occurred in nearshore and central areas of Grande Bay, where the MLD was also shallow (10 m).

Nitrate, phosphate and silicate concentrations at three sampling depths over the study area are shown in Fig. 5. Nitrate values ranged 5–16.6 μM and were lowest at surface and middle depths at outer stations on PD transect (St 41–43) and in the Grande Bay area (St 72 and 73). Highest values were recorded at all depths along BUR transect. Phosphate concentrations ranged from 0.46 to 1.84 μM; highest values were found at surface and mid depths along BUR transect and at the outermost stations on the PD section, within the deeper layer. Concentrations were lowest at coastal stations on PD, SF, GB and MAG transects, in all cases within the lower layer. At surface and intermediate depths, phosphates were relatively lower in central Grande Bay and approaching the shelf-break on PD transect. Silicate concentrations ranged 0.48–5.86 μM. Relatively higher values were recorded along BUR transect at mid and lower depths, although maximum concentrations occurred along MAG transect. Minimum values were found along PD and SF transects at surface and within the lower layer, while within the mid layer the lowest values occurred in the Grande Bay area. N/P ratios were generally within the range of 8–10:1, with values of >13:1 found at a few locations. Lowest ratios (6–7:1) were recorded in the GB and SFP areas, suggesting that a high phytoplankton activity was taken place. Nutrient sharpest vertical gradients were observed in central Grande Bay and approaching the shelf-break offshore PD transect, which would also reflect phytoplankton consumption in the upper layers. Overall N/P ratios over the study area approximated the optimal Redfield ratio (16:1) indicating no N or P limitation of primary production. 3.2. Chlorophyll a distribution Sea surface and vertical distribution of total Chl a over the study area have been reported elsewhere (Bianchi et al., 2009; Lutz et al., 2010). In short, values at surface varied widely, from 0.5 to 28.6 mg m − 3, although most of the southern shelf showed intermediate values, between ca. 0.8 and 2.0 mg m − 3. Concentrations were particularly high in the Grande Bay area at about 80 km from the coast (28.6 mg m − 3, at additional station located between St 72 and St 73), but also further offshore towards southeast (4.6 mg m − 3, St 67), and at ca. 47°S on the shelf-break (7.7 mg m − 3, St 41). Lowest concentrations (b0.8 mg m − 3) were recorded southwards in coastal and offshore waters at about 54°S, and beyond the shelf-break at

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Fig. 5. Distribution of nitrate, phosphate and silicate at three depths (surface = 0 m, mid = 20 m ± 10 and lower = 70 m ± 40) over the southern Patagonian shelf during early spring.

about 47°S (Fig. 6A). The Chl a patch in the Grande Bay area extended down 10 m between St 71 and St 73, with values decreasing abruptly towards either coast or offshore or deeper. The distribution of size-fractioned Chl a (Fig. 6B) showed two spots in particular where the contribution of the >5 μm size fraction was remarkably high, i.e., offshore 47°S , near the 200 m isobath with values between ca. 2–8 mg m − 3 representing 74–95% of total concentration, and in mid Grande Bay (73–85%). A strong gradient of the >5 μm size fraction was evident across the Chl a patch in Grande Bay, with the proportion of larger Chl a decreasing abruptly from St 71–72 to 74, from 77–63% down to only 4%, respectively. Overall, at both sides and below the Chl a patch, the contribution of smaller phytoplankton (b5 μm) to total Chl a was 50–100%. 3.3. Phytoplankton and protozooplankton assemblages Most complete data matching simultaneous sampling of all plankton size fractions concerned conditions at surface. Thus, we used only

surface data when searching for patterns of the small-sized plankton community, i.e. >ca. 1–200 μm (bacterioplankton excluded). From this data set, nonetheless, no clear grouping of locations was disclosed through either cluster or MDS analysis. Perhaps a finer taxonomic resolution within this fraction would have revealed subtle differences in their community structure that our approach did not. It is also commonly recognized, nevertheless, that the identification of small plankton entails still serious difficulties (Vaulot et al., 2008). The composition and abundance of plankton size-fractions of b200 μm were analyzed after their trophic condition, i.e., autotrophs and heterotrophs/phagotrophs (Table 2). The b2 μm size fraction (Fig. 7A) comprised cyanobacteria of the genus Synechococcus and eukaryotes belonging mainly to coccal chlorophytes. Their abundance was highest in the middle shelf sector near 100 m depth. The autotrophic compounds of the 2–5 μm fraction (Fig. 7B) were fairly diverse: centric diatoms, coccal and flagellate chlorophytes (Pyramimonas sp.), haptophytes such as Chrysochromulina-like flagellates and the coccolithophorids Emiliania huxleyi and Gephyrocapsa oceanica. This

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size-fraction was distributed all over the study area but the highest concentration (18 · 106 cells L − 1) was recorded in a sector of Grande Bay (St 74), where a small centric diatom (3 μm), Minidiscus trioculatus, was blooming. Dinoflagellates, diatoms and euglenophytes built up the autotrophic >5–10 μm size fraction (Fig. 7C). This group was less

Table 2 Dominant taxa in the several size-fractions of phytoplankton and protozooplankton within the range of 0.2–200 μm. Size-fraction b 2 μm Autotrophs

Class/Morphological groups/Taxa Cyanophyceae: Synechococcus spp. Chlorophyceae: coccal cells

2–5 μm Autotrophs

Prasinophyceae: Pyramimonas sp. Cryptophyceae: species of genera Hemiselmis or Plagioselmis Prymnesiophyceae: Emiliania huxleyi, Gephyrocapsa oceanica, Chrysochromulina-like flagellates Bacillariophyceae: Minidiscus trioculatus Heterotrophs Unidentified flagellates, unidentified naked-ciliates 5–10 μm Autotrophs

Euglenophyceae Bacillariophyceae Dinophyceae Heterotrophs Dinophyceae Unidentified flagellates, unidentified dinoflagellates

10–20 μm Autotrophs

Dinophyceae: Prorocentrum minimum, unidentified thecate dinoflagellates Bacillariophyceae: pennate diatoms Cryptophyceae Dinophyceae Unidentified flagellates, unidentified coccoid cells Heterotrophs Unidentified flagellates 20–200 μm Autotrophs

Bacillariophyceae: Thalassiosira cf. oceanica and Thalassiosira spp., Pseudo-nitzschia spp. (seriata and pseudodelicatissima complexes), Chaetoceros spp. (sect. Curviseta and Oceanica), Skeletonema costatum, Paralia sulcata, Thalassionema nitzschioides, Stephanopyxis turris, Asterionellopsis glacialis, Fragilariopsis spp. Heterotrophs Dinophyceae: Protoperidinium capurroi, Amphidinium spp., unidentified naked dinoflagellates

diverse and abundant than the previous one, and distributed mainly in deeper waters near the shelf-break. The taxonomy of the smallest heterotrophic organisms in the 2–5 μm fraction is rather complex and poorly known. Their maximum abundances were recorded offshore the PD transect, approaching the shelf-break (Fig. 7F). The heterotrophic part of the >5–10 μm size fraction (Fig. 7G) comprised non-identified dinoflagellates and flagellates. This group was not widely distributed over the study area but mainly in offshore waters. Within the larger nanoplankton (>10–20 μm) and microplankton (>20–200 μm) fractions, photosynthetic groups included diatoms, dinoflagellates and a miscellany of taxonomic groups such as silicoflagellates and euglenophyceans. Heterotrophs/phagotrophs included dinoflagellates, naked and loricate ciliates and, occasionally, foraminifers, amoebae, etc. Within the photosynthetic nanoplankton >10–20 μm size fraction (Fig. 7D), an exceptional proliferation (up to 10 · 10 6 cells L − 1) of the dinoflagellate Prorocentrum minimum was recorded at the middle shelf sector of Grande Bay. This bloom was almost monospecific, since P. minimum cells constituted >99% of the plankton community at the upper levels of the water column. Other autotrophic taxa of this size fraction were present at the whole area in a much lower abundance (several orders of magnitude) and comprised pennate diatoms, cryptophytes, coccoid forms, phytoflagellates and thecate dinoflagellates. Another bloom was detected at the shelf break sector at 47°S (Fig. 7E), this time caused by diatoms of the microplankton (>20– 200 μm) size fraction. One species of the genus Thalassiosira (cf. T. oceanica) was the main component (~ 90%, 4.3 · 10 6 cells L − 1) of the planktonic community, of which various species of Pseudo-nitzschia and Chaetoceros were secondary components. Less abundant microplankton spots built up also by diatoms of genera Skeletonema, Paralia, Thalassionema, Stephanopyxis, Asterionellopsis, Chaetoceros, Thalassiosira, Fragilariopsis and Pseudo-nitzschia were recorded in Grande Bay and at the BUR transect. Dinoflagellates and non identified flagellates constituted the main taxa of nanoplanktonic (>10–20 μm) heterotrophs. Within this category most of the area showed a low abundance (b103 cells L − 1) with relatively larger cell concentrations in Grande Bay (Fig. 7H). Heterotrophic microplankton (Fig. 7I) also showed a significantly lower abundance than the photosynthetic fraction, with a predominance of heterotrophic/ phagotrophic dinoflagellates on ciliates. Protoperidinium capurroi, Amphidinium spp. and other unidentified naked dinoflagellates were

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Fig. 7. Surface distribution of phytoplankton and protozooplankton size fractions off southern Patagonia during early spring. A, Autotrophs b2 μm from epifluorescence counts; B–E, Autotrophs 2–5 μm, > 5–10 μm, >10–20 μm and >20–200 μm size fractions from Utermöhl counts; F–I, Heterotrophs 2–5 μm, > 5–10 μm, >10–20 μm and >20–200 μm size fractions from Utermöhl cell counts. Values at the bottom right corner in all maps refer to maximum numbers. Note the different orders of magnitude recorded for each fraction, particularly differences between autotrophs and heterotrophs. In 6B, the diamond symbol and label below (18.5 · 106 cells L− 1) refer specifically to the huge abundance of the small diatom Minidiscus trioculatus (~3 μm) at St. 74 (out of the scale illustrated with open circles, max. 106 cells L− 1).

the main components of the heterotrophic community associated with the Thalassiosira bloom recorded in the shelf-break sector at 47°S.

3.4. Mesozooplankton community structure No effect of depth on the mesozooplankton community composition was found between the two sampled strata (one-way ANOSIM, Global R = −0.017, p b 0.68). Hence, subsequent analyses were applied to depth-integrated abundances estimated for the whole sampled column (Table 1). We identified distinct geographical patterns in the distribution of species across shelf. Three groups of stations were recognized by cluster and MDS analysis, which closely corresponded with the Inner (N = 10), Mid (N = 7) and Outer (N = 6) sectors of the shelf (Fig. 8). The MDS ordination yielded a stress value of 0.12, suggesting a satisfactory geographical allocation of groups. Assemblages proper of the

inner and middle shelf overlapped slightly but were well separated from the outer shelf community. The analysis of similarities (ANOSIM, Table 3) showed that latitudinal differences in the mesozooplankton community structure were weakly significant (defined as a priori groups after ‘Transects’ factor, Global R = 0.169; p b 0.04). Only stations grouping at ca. 51°S (GB transect, Fig. 1) proved clearly different, yet overlapping, from those at ca. 55°S (BUR transect, Fig. 1). The remaining groupings were either not separable or barely separable at the most (e.g. stations at 53°S from those at 55°S, MAG vs BUR; stations at 47°S from those at 51°S, PD vs GB, Fig. 1). Negative values of R in the comparisons PD vs BUR and SFP vs GB are indicative of larger differences withingroups than between-groups. Typical species (SIM/SD ratio > 3 in SIMPER output, results not shown) of the inner shelf were adults and late copepodids of Drepanopus forcipatus, while the mid shelf sector was characterized by females and copepodids 4–5 of Ctenocalanus vanus, the amphipod

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43

Fig. 8. Grouping of stations by the cluster analysis based on the Bray–Curtis similarity matrix created from double-root transformed data of mesozooplankton abundances integrated over the water column (above panel). The here identified three groups of stations correspond to symbols used in the MDS plot (below left panel), which are geographically located on the map (below right panel).

Themisto gaudichaudii and the chaetognath Sagitta tasmanica. Unlikely, the outer shelf sector was characterized by a variety of taxa, which exhibited in accordance the lowest average intra-group similarity (35.8, Table 4). The highly abundant euphausiid eggs and larvae present therein was yet a remarkable feature of this sector as opposed to the low abundances of any other taxa (Table 4, Fig. 10A, B). Drepanopus forcipatus adults and stages 4–5 accounted together for 69.6% of the average similarity of the inner shelf pattern (58.7). They were also abundant in the mid shelf sector, although Ctenocalanus vanus females and copepodids 4–5 occurred less abundantly but more consistently throughout most locations (Fig. 9A). Thus, the standard deviations of their contribution to average similarity (62.8, Table 4) Table 3 Mesozooplankton community structure. Analysis of similarities along the southern Patagonian shelf (ANOSIM tests). Along shelf Factor: Transects Global R: 0.17; Significance Level: 0.037 Groups PD, SFP PD, MAG PD, BUR PD, GB SFP, MAG SFP, BUR SFP, GB MAG, BUR MAG, GB BUR, GB

R 0.07 0.10 − 0.06 0.35* 0.07 0.52 − 0.22 0.46* 0.04 0.62*

Table 4 Average depth-integrated abundance (ind m− 2) within station groupings across shelf of mesozooplankton species/taxa/stages with highest contributions to average within-group similarity and between-group dissimilarity (SIMPER analysis). Names and values in bold refer to the best discriminating taxa between groups (Diss/SD > 2 in SIMPER analysis) and highest average abundances across all shelf areas, respectively. Species/Taxon

Inner shelf

Mid shelf

Outer shelf

N = 10

N=7

N=6

Similarity = 58.6 Similarity = 62.8 Similarity = 35.8 Drepanopus forcipatus 1–3 Drepanopus forcipatus 4–5 Drepanopus forcipatus F Drepanopus forcipatus M Ctenocalanus vanus 4–5 Ctenocalanus vanus F Ctenocalanus vanus M Clausocalanus brevipes 4–5 Clausocalanus brevipes F Clausocalanus brevipes M Clausocalanus laticeps 4–5 Clausocalanus laticeps F Calanus simillimus F Oithona helgolandica Oithona atlantica Themisto gaudichaudii Sagitta tasmanica Sagitta gazellae Crustacea larvae Euphausiid eggs Euphausiid larvae Thysanoessa spp.

1322 61,261

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0 0.8

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10,364 1542 751 953 368 288

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822 216 0 63 4 377 65 174 19 0 33 90 315 0

41 1.9 131 74 22 8.9 0.5 5 1.5 1.7 5 32,908 197. 3 1.1

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Fig. 9. Distribution of copepod populations off southern Patagonia during early spring. Note distinct abundances between small Clausocalanidae species (A) and large Calanidae species (B). Values refer to maximum depth-integrated abundances recorded over the study area. Open circle and label below (940,000 ind m− 2) refer specifically to the huge abundance of Drepanopus forcipatus at St. 72 (out of the scale illustrated with filled circles, max. 165,000 ind m− 2).

were low, and the SIM/SD ratios relatively higher, typifying better the mid-shelf sector. This was also the case of Themisto gaudichaudii and Sagitta tasmanica (Table 4, Fig. 10F and G). The two copepod species mentioned above plus Clausocalanus brevipes females were also good discriminating species, mainly because of their consistently distinct abundances across the three sectors (DISS/SD > 2 in SIMPER output, results not shown) (Table 4, Fig. 9A).

3.5. Copepods abundance, distribution and population structure Copepods largely dominated the >200 μm fraction (91–99%) over most of the study area. Exceptions were the northernmost (PD) and southernmost (BUR) transects where either euphausiid eggs or euphausiid juveniles and adults were more abundant, mainly over the outer shelf sector, under the influence of the Malvinas Current. Relatively small Clausocalanidae species were strikingly more abundant than large Calanidae species, with Drepanopus forcipatus as absolute dominant. This later and Calanus australis were highly abundant in the inner and mid shelf sector and decreased offshore, while Clausocalanus brevipes, Ctenocalanus vanus, Neocalanus tonsus (only C5) and Calanus simillimus showed an opposite trend (Fig. 9A, B). Small cyclopoid copepods such as Oithona spp. did occur, mainly over the middle shelf, but they were clearly undersampled by the 200 μm mesh size, since maximum abundance was 1000 ind m − 2 (cf. Antacli et al., 2010). Much less abundant or rarely occurring species were Metridia lucens, Rhincalanus nasutus, Eucalanus longiceps, Centropages brachiatus, Pleuromamma robusta, Oithona atlantica and Oncaea spp. This dissimilar distribution and abundance of both small and large copepod species, mainly across-shelf, was indeed reflected in the community patterns described earlier (Fig. 8). The Drepanopus forcipatus population was equally distributed through the water column and dominated by late copepodids 4 and 5 and adult females, while the Calanus australis population was slightly more abundant within the lower layer and dominated by copepodid stage 5. Clausocalanus brevipes and Ctenocalanus vanus populations were rather homogeneously distributed in the vertical, with adult females dominating in both cases. On the contrary, Calanus simillimus C5 were more abundant in the lower layer while adult females seemed to stay in the upper layer.

Abundance of both size copepods was remarkably higher in the Grande Bay area, where the Prorocentrum minimum bloom was proceeding. 3.6. Larger zooplankton Groups at higher trophic levels such as euphausiids, amphipods and chaetognats were also differently distributed, mainly acrossshelf but also along-shelf (Fig. 10). A spawning event of euphausiids was taking place on the shelf-break to the north of the study area (Fig. 10A), co-occurring with the Thalassiosira sp. bloom (Fig. 7E). Otherwise, the abundance of either their larvae (Fig. 10B) or adults was much lower (although likely underestimated because of the sampler and sampling depth). Adults of Euphausia vallentini (Fig. 10C) distributed mostly to the south of the study area while E. lucens (Fig. 10D) occurred to the north, and Thysanoessa gregaria (Fig. 10E) was indistinctly present along the area. The three species occurred only at the middle- and outer-shelf sectors. Euphausia vallentini and Thysanoessa gregaria were more abundant in areas close to the shelf-break while Euphausia lucens was distributed more abundantly in middle-shelf waters off Grande Bay. The amphipod Themisto gaudichaudii was relatively much more abundant than euphausiids and chaetognaths, and distributed to the south of ca. 49°S, mainly at the middle-shelf sector (Fig. 10F). The chaetognaths Sagitta tasmatica (Fig. 10G), S. gazellae (Fig. 10H) and Eukronia hamata (Fig. 10I) occurred only from 50°S southwards, being the former relatively much more abundant on the MAG transect; the rest of the species reached higher abundances at BUR transect. 3.7. Environmental variation In characterizing the environment associated to plankton communities, a PCA ordination of sampling sites was performed on some relevant hydrological and chemical variables selected a priori, i.e., temperature, salinity, thermal and saline stratification, Chl a > 5 μm, nitrate and silicate concentrations, and mixing layer depth (MLD). Significant latitudinal differences were found in day-light length (hours), increasing southwards (after the vernal equinox). However, this variable proved to be unimportant in our PCA analysis and was removed.

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

68°

W 47°

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55° S 58°

Fig. 10. Distribution of euphausiid and chaetognath populations off southern Patagonia during early spring. A, Euphausiid eggs; B, Euphausiid larvae; C, Euphausia vallentini adults; D, Euphausia lucens adults; E, Thysanoessa gregaria adults; F, Themisto gaudichaudii; G, Sagitta tasmanica; H, Sagitta gazellae; I, Eukronia hamata. Values at the bottom right corner in all maps refer to maximum numbers. Note the different order of magnitude recorded for euphausiid eggs in particular.

Environmental axes PC1 and PC2 accounted together for the 66.4% of variation for the array of stations in Fig. 11; significantly correlated variables for each axis are shown in Table 5. First axis is one of increasing salinity, nutrient concentration and saline stratification, but decreasing temperature. Most of the stations actually separated along PC2, that is, along the axis of increasing thermal stratification and chlorophyll > 5 μm but decreasing MLD and nutrients. Axis PC3 contributed to explain an additional 10% of total variation, being decreasing Chl a > 5 μm concentration the variable that largely accounted for most of it. Amongst significant environmental variables (Table 5), salinity, saline and thermal stratification, nutrients and changes in Chl a > 5 μm concentration, were the properties best explaining the mesozooplankton patterns (BIO-ENV analysis, Table 6). As mentioned earlier, no distinct patterns of phytoplankton and protozooplankton assemblages were apparent when the b200 μm plankton community structure was considered as a whole. However, looking specifically at the optimal food size for copepods (>10 μm),

communities were slightly different across the shelf (i.e., for the same site groupings as those disclosed by cluster analysis from mesozooplankton data, cf. Fig. 8). That is, food assemblages within the inner- and middle-shelf were alike but somehow distinguishable from the outer-shelf community (Table 7). Further examination of these patterns through a MDS plot (Fig. 12) indicates that at far apart sites 71 and 72 within the inner sector the Prorocentrum minimum bloom was taking place, while at sites 41, 42 and 43 within the outer sector Thalassiosira sp. was blooming (cf. also Fig. 7). It is also evident the overlapping of sites located in the inner- and middle-shelf sectors, which share about the same composition and abundances of potential food larger than 10 μm (Fig. 7, Table 8). The influence of phytoplankton and protozooplankton assemblages on the mesozooplankton abundance and composition was tested through the RELATE routine, on the basis of size and trophic condition of the organisms. Significant correlations were found particularly with large autotrophs and heterotrophs (Table 9).

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M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

3

Thermal stratification Chlorophyll >5 µm Saline stratification Temperature

72 43 42

2 74

41 Salinity Silicate Nitrate Saline stratification Thermal stratification Chlorophyll >5 µm

71

1 75

Temperature MLD 0

PC2

5251 69 47

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59

57 -2

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60

0

1

2

3

4

PC1 Inner-shelf

Middle-shelf

Outer-shelf

Fig. 11. PCA ordination of environmental variables at mesozooplankton sampling stations over the southern Patagonian Shelf during early spring. PC1 (38.8% of variation): + 0.506 salinity + 0.396 silicate + 0.390 nitrate + 0.370 saline stratification + 0.310 thermal stratification + 0.207 Chl a > 5 μm − 0.350 temperature − 0.192 mixing layer depth (MLD). PC2 (27.6% of variation): + 0.475 thermal stratification + 0.379 chlorophyll a > 5 μm + 0.256 saline stratification + 0.251temperature, − 0.483 MLD − 0.375 nitrate − 0.349 silicate − 0.081 salinity. Highly correlated variables (P b 0.01) with environmental axes are in bold (Pearson correlation coefficients in Table 5). The symbols of zooplankton groupings as they were disclosed by cluster analysis (see Fig. 8) were superimposed on station labels.

4. Discussion According to bathymetry and physical processes that control the water properties, the southern Patagonian Shelf can be divided into inner, middle and outer sectors. These are, respectively, under the prevalent influence of water masses typically defined by their saline content (Bianchi et al., 1982). In turn, the contrast between dissimilar salinity waters generates fronts of varied intensity. Mesozooplankton patterns were found to be distinctly defined across-shelf (Fig. 8), with typical communities for each sector that mirrored the distribution of water masses and fronts to a significant degree (Fig. 3). In accordance, a combination of environmental variables such as salinity, saline and thermal stratification, nutrients and changes in Chl a > 5 μm concentration, best explained mesozooplankton distribution (BIO-ENV analysis, Table 6). These water mass characteristics are all factors expected to define the niche of plankton communities both directly or indirectly, conditioning preferred depths, food availability and feeding modes. Salinity was a major factor detaching the inner- and middle-shelf groups from the outer mesozooplankton community (cf. Fig. 11, PCA ordination of sampling sites allowing for their environmental Table 5 Significant Pearson correlation coefficients between PCA axes and environmental variables. Percentage of variance accounted for by each component is shown in parentheses. Critical values for correlation coefficients: 0.623 (P b 0.01) and 0.497 (P b 0.05, df = 14). Environmental variables

PC 1 (38.79%)

Temperature Salinity Saline stratification Thermal stratification Chlorophyll a > 5 μm Nitrate Silicate Mixing layer depth

− 0.62** 0.89** 0.65** 0.55* 0.69** 0.70**

PC2 (27.58%)

PC3 (10.13%)

features; Table 5). Thus, it appears that the Magellan salinity front separated the former two from the outer group, with the middleshelf group comprising the transitional stations located just at the beginning of the saline gradient (e.g., outer stations on GB transect, Figs. 2C, D and 8). Most sites in the inner-shelf group were characterized by relatively higher thermal stratification and a shallower mixing layer than those included in the middle-shelf group. However, the (weak) splitting of the assemblages proper of the inner and middleshelf sectors was more likely related to differences in the incipient phytoplankton activity over the shelf, as it is reflected in increasing nutrient consumption along with higher chlorophyll > 5 μm concentrations at locations of the inner- relative to the middle-shelf mesozooplankton groups. Distinct phytoplankton activity would also explain the detachment of the northern and southern subgroups over the outer-shelf sector (Fig. 11). This is further supported by our PCA analysis which demonstrate the large weight of chlorophyll > 5 μm (along axis PC3) in explaining the total environmental variation (Table 5). Therefore, it seems likely that the distribution of mesozooplankton assemblages was determined by niche adaptation. The species composition and abundance of the zooplankton assemblages are in accordance with the regional overall patterns previously described. During spring, biomasses are mostly dominated by copepods, while during late summer and early autumn amphipods and euphausiids become more abundant inshore and offshore,

Table 6 Environmental influence on mesozooplankton assemblages (BIOENV analysis). Coefficients of Spearman rank correlation between selected variables and the mesozooplankton pattern in Fig. 7. Abiotic factor

0.71** 0.56* − 0.57* − 0.52* − 0.72**

− 0.69**

Spearman rank correlation

Salinity, saline and thermal stratification, silicate 0.762 Salinity, saline and thermal stratification, nitrate, silicate 0.751 Salinity, saline and thermal stratification, chlorophyll a > 5 μm, 0.746 silicate

M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51 Table 7 Community structure of available potential food for copepods (>10–200 μm) over the southern Patagonian shelf. Analysis of similarities (one-way ANOSIM) across the same three site groupings as disclosed for mesozooplankton (inner, mid and outer shelf sectors). Phytoplankton and protozooplankton cell counts (cells L− 1) at three depths were integrated through the water column taking into account zooplankton sampling strata. A similarity matrix was created on the basis of the Bray–Curtis similarity index on these double-root transformed data of abundance (cells m− 2).

Table 8 Potential food >10–200 μm over the southern Patagonian shelf during early spring. Average (depth integrated) abundance (cells m− 2) of phytoplankton and protozooplankton size-fractions within the same site groupings as for mesozooplankton (Fig. 7). Sizefractions and values in bold refer to the best discriminating taxa between groups (Diss/ SD > 3 in SIMPER analysis) and highest average abundances across all shelf areas, respectively. Functional size-fraction

Factor: stations grouping after mesozooplankton cluster (Fig. 7) Global R: 0.211; Significance Level: 0.011 R

OUTER, MID OUTER, INNER MID, INNER

0.388* 0.356* 0.000

respectively (Sabatini and Álvarez Colombo, 2001). Amphipods are almost exclusively represented by the hyperiid Themisto gaudichaudii (Ramírez and Viñas, 1985), and Euphausia lucens, Euphausia vallentini and Thysanoessa gregaria are the most abundant euphausiids (Ramírez, 1971, 1973). Same as in summertime, a few species dominate the spring copepod community, particularly in the inner and middle shelf sectors, where Drepanopus forcipatus is overwhelmingly dominant along with Calanus australis and other small clausocalanids, though these latter to a much lesser extent (Sabatini, 2008a,b). Diversity increases in offshore direction, mainly due to the incorporation of large calanoids (Ramírez and Sabatini, 2000). Small cyclopoids are also abundant and widely distributed over the southern Patagonian shelf (Antacli et al., 2010). The relatively low number of mesozooplankton species in the southern Patagonian shelf may be associated with its highly seasonally pulsed production cycle, typical of cold-temperate ecosystems. It appears that species richness decreases as more seasonally pulsed becomes the availability of food resources, because a few number of more generalist taxa become dominant (Angel, 1993, 1997). A similar explanation has been suggested for the low diversity of fish assemblages at the Southern Shelf-Break and Magellan fronts (Alemany et al., 2009). We had hypothesized that differential sea surface warming along such a latitudinally extended area (47°S–55°S) and increasing solar radiation during the spring, would promote a dissimilar establishment of the seasonal thermal stratification and, hence, a diversity of habitats for plankton communities. For instance, the PD transect lies within an area of earlier beginning of the sea surface warming relative to all other transects, which cross a rather homogenous area in terms of surface heat flux and hence warming/cooling (Rivas, 2006). Against

Stress: 0.14 52

74

51 47 50

57

59 55 53 56 54 61

38

60

68 75 69

43

71 72

Inner-shelf

Mid-shelf

Outer-shelf

N = 10

N=7

N=6

Similarity = 61 Similarity = 73 Similarity = 69

Groups

49

47

41 42

Fig. 12. Potential food environment across the Inner, Mid and Outer shelf sectors (as disclosed for mesozooplankton, same symbols as in Fig.7). MDS plot from a similarity matrix created on the basis of the Bray-Curtis similarity index on double-root transformed data of potential food abundances (cells m− 2). Larger than 10 μm phytoplankton and protozooplankton cell counts (cells L− 1) at three depths were integrated through the water column taking into account zooplankton sampling strata.

Diatoms 10–20 μm Autotrophic dinoflagellates 10–20 μm Non-identified autotrophs 10–20 μm Heterotrophic dinoflagellates 10–20 μm Ciliates 10–20 μm Non-identified heterotrophs 10–20 μm Diatoms > 20 μm Autotrophic dinoflagellates > 20 μm Non-identified autotrophs > 20 μm Heterotrophic dinoflagellates > 20 μm Ciliates > 20 μm Non-identified heterotrophs > 20 μm

26,904 9,320,073

33,178 7004

11,727 15,2403

16,950

16,368

9384

18,470

7744

339

1670 b1

1847 0

1566 0

486,842 9631

922,920 23,211

25,027,428 113,449

8346

32,837

44,415

26,627

42,900

203,072

21,361 221

27,174 6679

4138 551

these expectations, the biological patterns were not clearly different along the shelf, even when more than 700 km separate the northernmost (PD) from the southernmost sampling transect (BUR). The reason was that at the time of the cruise fairly homogeneous thermal conditions were still present over most of the shelf, with typical thermoclines not well established yet. Climatological studies on satellite chlorophyll in the region (Rivas et al., 2006; Romero et al., 2006) show that down to ca. 48°S the onset of the spring bloom propagates from low to high latitude, and from the outer (beginning in October) to the inner shelf (beginning in November), likely following the establishment of the seasonal thermal stratification. Further southwards, in contrast, the bloom seems to begin in northern Grande Bay in October, spreading N-NE during November and December, in coincidence with the predominant mean flow (Palma et al., 2008). In situ Chl a data here and satellite (Lutz et al., 2010) fit well this climatological picture. We found particularly high surface concentrations of total Chl a in the Grande Bay area and at ca. 47°S on the shelf-break, with a large contribution of the >5 μm fraction (70–90%) at both locations. Microscopic cell counts proved that the diatom Thalassiosira cf. oceanica. and the dinoflagellate Prorocentrum minimum were blooming in offshore waters at 47°S and in Grande Bay, respectively. Likely “new” production (Dugdale and Goering, 1967) based on nitrate newly arrived from outside the productive layer was taking place at those sites, as relatively large cells were blooming and lower nitrate concentrations were recorded concurrently. Within the same area, however, also the small diatom Minidiscus trioculatus (~3 μm) was blooming closer to the coast (St 74, GB transect — Fig. 7B) and next to the Prorocentrum bloom. At that location, Minidiscus trioculatus made up the 90% Chla b5 μm (Fig. 6B), with cell concentrations of >10 7 cells L − 1. Although the composition of this small-sized fraction has been at present barely studied, those numbers are in good agreement with the species' abundance during upwelling situations (Buck et al., 2008). Both spots of enhanced (large) phytoplankton biomass would relate to the strong influence of the Malvinas Current on the shelf. The Thalassiosira bloom occurring far offshore at ca. 47°S is likely linked to the input of new nutrients straight from the shelf-break upwelling, in coincidence with the relatively earlier beginning of the sea

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M.E. Sabatini et al. / Journal of Marine Systems 94 (2012) 33–51

Table 9 Matching mesozooplankton community structure and food environment. RELATE outputs for Bray–Curtis similarity matrices of mesozooplankton (ind m− 3) and sizefractioned phytoplankton and protozooplankton (cells L− 1). Only surface data, double-root transformed; ρ = coefficient of Spearman rank correlation. Food type and size-fraction

Spearman rank correlation

N

Phytoplankton + protozooplankton All size-fractions (AUT + HET > 20; AUT + HET > 10–20; AUT + HET > 5–10; AUT + HET 2–5) Phytoplankton all size-fractions (AUT > 20; AUT > 10–20;AUT > 5–10; AUT 2–5) Protozooplankton all size-fractions (HET > 20; HET > 10–20;HET > 5–10; HET 2–5) Phytoplankton + protozooplankton > 10 μm (AUT + HET > 20; AUT + HET > 10–20) Phytoplankton > 10 μm (AUT > 20; AUT > 10–20) Protozooplankton >10 μm (HET > 20; HET > 10–20) Food > 10–20 μm (AUT + HET > 10–20) Phytoplankton > 10–20 μm (AUT > 10–20) Protozooplankton > 10–20 μm (HET > 10–20) Food > 20 μm (AUT + HET > 20) Phytoplankton > 20 μm (AUT > 20) Protozooplankton > 20 μm (HET > 20) Phytoplankton + protozooplankton b 10 μm (AUT + HET > 5–10; AUT + HET 2–5) Phytoplankton b 10 μm (AUT > 5–10; AUT 2–5) Protozooplankton b 10 μm (HET > 5–10; HET 2–5) Food > 5–10 μm (AUT + HET 5–10) Phytoplankton > 5–10 μm (AUT > 5–10) Protozooplankton > 5–10 μm (HET > 5–10) Food 2–5 μm (AUT + HET 2–5) Phytoplankton 2–5 μm (AUT 2–5) Protozooplankton 2–5 μm (HET 2–5)

ρ = 0.232*

19

ρ = 0.191 n.s. ρ = 0.128 n.s. ρ = 0.235*

19

ρ = 0.225*

23

ρ = 0.134 n.s. ρ = 0.104 n.s. ρ = 0.129 n.s. ρ = − 0.077 n.s. ρ = 0.356 **

23

23

ρ = 0.353 **

23

ρ = 0.226 *

23

ρ = 0.158 n.s. ρ = 0.089 n.s. Many absences Non-valid test Many absences Non-valid test Many absences Non-valid test Many absences Non-valid test ρ = 0.117 n.s ρ = 0.015 n.s Many absences Non-valid test

19

19 23

23 23 15

19 19 19 19 19 19 19 19

surface warming at that latitude. As regards the Prorocentrum minimum bloom in Grande Bay, the supply of inorganic nutrients to the upper layers into this area may be associated to intrusions of nutrient-rich waters of Malvinas Current onto the shelf. Some observations and recent numerical simulations postulate the spreading, onshore and downward, of cold and denser waters from the shelf-break upwelling (Matano et al., 2010). The nutrients carried by these waters would certainly add to the nutrient pool, which may be largely in excess for most of the productive season, as indicated by the N/P ratios we found (ca. 13–14). Diatoms are often the dominating group during the spring bloom in temperate areas, while dinoflagellates are only present in low numbers (Margalef, 1978; Smayda and Reynolds, 2003). We cannot know for certain from our narrow sampling window whether the Prorocentrum minimum bloom in Grande Bay occurred occasionally at this time of the year or if this is a recurrent feature in this sector of the southern Patagonian shelf. In early summer 2003, for instance, a bloom by the diatom Chaetoceros debilis (3· 106 cells L− 1; 19 mg m − 3 Chl a) was recorded in the very same area (Almandoz et al., 2007; Schloss et al., 2007). Recent observations indicate that mechanisms other than heat input, for example surface freshening by river runoff, can also

contribute to the upper ocean stratification and trigger spring blooms (Labry et al., 2001; Lucas et al., 1998; Waniek et al., 2005; Wu et al., 2008). In coincidence, our findings indicate that, comparatively with the surrounding shelf, the water column was slightly stratified in the Grande Bay area, with a locally important contribution of low salinity from river runoff (Fig. 4).The advantage of dinoflagellates possessing UV-absorbing compounds to predominate in well-stratified surface waters under high solar irradiances in spring has been proposed (Carreto et al., 1990). Absorption spectra of phytoplankton at the Grande Bay bloom showing a strong signal of UV-absorption (Segura, unpublished data) give further support to this hypothesis. Mesozooplankton community structure and food environment patterns matched weakly, suggesting a poor coupling between consumers and their prey communities (RELATE analysis, Table 9). Nevertheless, daytime of zooplankton collection — at daylight hours on several occasions, may have biased our results to some extent. Nycthemeral feeding patterns are for instance recognized for copepods, indicating higher rates in the dark than during daylight periods (e.g., Barquero et al., 1998). In any case, significant correlations were found particularly with large autotrophs and heterotrophs. Prey selection in planktonic predators is primarily governed by prey size (Kiørboe, 2008) and it is widely admitted that mesozooplankton broadly controls phytoplankton (Steele, 1974) and protozooplankton in the 5–200 μm range (Calbet and Landry, 1999, 2004). Larger contribution to correlation values between mesozooplankton and >10 μm potential food communities was likely due to a few and rather local events where strong coupling certainly occurred. In the Grande Bay area the Prorocentrum bloom seemed to be well exploited by copepod populations which were actively feeding and reproducing (Antacli et al., 2011), while at the shelf-break off Puerto Deseado at 47°S the Thalassiosira bloom co-occurred with a euphausiid spawning event. Euphausiids are primarily herbivorous when phytoplankton is abundant (Mauchline and Fisher, 1969) and the seasonal timing of spawning peaks usually accompanies peaks in phytoplankton biomass (Lu et al., 2003). The distribution of euphausiid eggs and larvae we found agrees with previous records by Montú (1977); ripe females of Euphausia vallentini, the species most widely distributed during this study (Fig. 10C), are reported to increase in early spring (October) (Ramírez and Dato, 1983). Beyond the sampling constraints we mentioned earlier, our results suggest that spatial segregation of adults and larvae of euphausiids probably occurred. Distribution of both larvae and adults are strongly associated with local circulation in other boundary current systems, where larger euphausiids aggregate preferentially in shelf-break upwelling centers (Décima et al., 2010; Lu et al., 2003). Late juvenile stages undergo strong diel vertical migration, while smaller larval and early juvenile stages are no- or weakly migratory (Lu et al., 2003). At the next trophic level, mostly juveniles of the amphipod Themisto gaudichaudii were the most abundant organisms amongst larger mesozooplankton. This is recognized as a key species within the coastal and inner sectors of the southern Patagonian shelf ecosystem, as it is a main prey for fish and squid species (Ivanovic and Brunetti, 1994; Sánchez, 1999; Ciancio et al., 2008, 2010; Padovani et al., 2010), and its populations develop depending on copepods as food (Ramírez and Viñas, 1985; Sabatini, 2008b and references therein). As for chaetognaths, the distribution and relative abundance of the species is consistent with the patterns described earlier (Casanova, 1999; Mazzoni, 1983, 1988). Chaetognaths are carnivorous, feeding mainly on copepods, but they also consume fish larvae and other micro- and mesozooplankton taxa (Feigenbaum, 1982; Sullivan, 1980); their preys differ throughout ontogeny (e.g., Pearre, 1981; Reeve, 1980). Sagitta tasmanica feeds almost exclusively on copepods in the upper layers at night, before moving to deeper waters to digest their food (Gibbons, 1992) and the consumed species seem to vary seasonally (Liang and Vega-Pérez, 1995). Eukrohnia

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hamata predates mainly upon small to medium sized copepods (Øresland, 1990, 1995), while Sagitta gazellae predates upon large copepods, other chaetognaths and euphausiids (Froneman and Pakhomov, 1998; Øresland, 1990). As predators, they have the potential to substantially affect their prey communities (e.g., Bonnet et al., 2010), but are also significant in the diet of predators at higher trophic levels (Brodeur et al., 2000; Cavalieri, 1963). Further single correlations between different categories of potential food resources and the abundance of the various mesozooplankton taxa could not be established (correlation matrix comprising all variables, results not shown). For instance, we found no significant correlations to validate the kind of trophic relationships reported above regarding larger zooplankton and copepods. This may be related to their varying positions in the water column, as observed for sibling species in the Irish Sea; Calanus spp. and Pseudocalanus elongatus show a flexible diel pattern, from none to significant — or even reverse migration, depending on the vertical position of chaetognaths Sagitta spp. and depth of the water column (Irigoien et al., 2004). The absence of other significant relationships would also suggest complex trophic interactions within the smaller plankton fractions. For example, a microbial loop may have co-occurred with the Thalassiossira bloom at the shelf-break, as suggested by the trophic sequence from smallest 2–5 μm heterotrophs to >20 μm microzooplankton (cf. Fig. 7A–C vs F–I). Bacteria were not assessed in our study but it is well known that bacterioplankton can grow using diatom exudates as substrate and hence built up the basis for the development of a microbial loop (Azam et al., 1983). On the other hand, the Minidiscus bloom appeared to be associated with 10–20 μm heterotrophic nanoflagellates (cf. Fig. 7B vs H), which are recognized as major grazers of small-sized diatoms (Sherr and Sherr, 2007). Our findings about plankton biomass as well as nutrient enhancement in the southern region of the Patagonian Shelf are consistent with recent model results and observations suggesting that the cross-shelf circulation pattern in this region is dominated by onshore intrusions and subsequent upwelling of nutrient-rich waters of the Malvinas Current. After their entrainment near 50°S, these dense waters sink below the lighter shelf waters and move to the southwest in the bottom layer where they are subsequently mixed into the upper layers by intense tidal forcing. In particular, the model results show intense inshore bottom velocities in the Grande Bay (Palma et al., 2008) and therefore an enhancement of the enrichment processes in this area is expected. As suggested, the impact of the shelf-break upwelling in southern Patagonia may thus extend well beyond the shelf-break region itself (Matano et al., 2010). 5. Summary and conclusions In this study we examined the structure of the spring mesozooplankton community in the southern Patagonian shelf and the relationships with the overall plankton community and hydrography. We identified a distinct geographical pattern in the distribution of zooplankton species across the shelf. Three groups of stations with a few typical species each were recognized. These groups corresponded closely with the inner, middle and outer sectors of the shelf and prevailing water masses. Mesozooplankton was mostly dominated by copepods, with small and large species differently distributed. The highest abundance of both size copepods was found in the Grande Bay area (~51°S), where a bloom of the dinoflagellate Prorocentrum minimum was taking place. Copepod populations were actively feeding on this bloom. To the north of the study area (~ 47°), highly abundant euphausiid eggs and larvae were recorded on the shelf break, cooccurring with a bloom of the diatom Thalassiosira cf. oceanica. Except for these locations, small-sized plankton (b10 μm) prevailed over the shelf. The mesozooplankton community structure and overall food patterns matched weakly, suggesting a poor coupling between large consumers and their prey communities at the time. Nevertheless,

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significant correlations were found particularly with large autotrophs and heterotrophs. At the same time, rather complex trophic interactions would likely take place within the smaller fractions. The described hydrological and plankton scenarios indicate an early stage in the plankton trophic calendar. Full zooplankton response to the spring phytoplankton bloom would be apparent only few months later, as shown by summer enhanced zooplankton biomass recorded in previous studies in the Grande Bay area (Sabatini, 2008a; Sabatini et al., 2000). On account of its biological richness and hydrographic complexity, understanding the biological processes involved in the carbon cycle and the physical forcing structuring plankton communities is, therefore, particularly significant in the southern Patagonian shelf. All the more being the region closely connected with the Southeastern Pacific and likely a main pathway for fluxes into the Southern Ocean (Lara et al., 2010; Matano et al., 2010). Acknowledgments We thank the crew and scientific staff on board the R/V ARA Puerto Deseado for their valuable help. Our special thanks to the chief scientist A. Piola, and to F. Vázquez and G. Sanahuja for zooplankton sampling. Nora Fernández Aráoz identified and counted zooplankton samples. We thank A. Jaureguízar for his helpful advice with some multivariate analysis. This work was financed by a grant from the United Nations Development Program — UNDP (ARG 02/018 BB61) to M.S. and R.A. and by the Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP). Additional funding was provided by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), PIP-5845/05 to M.S. Grants UNDP ARG 02/018 BB46 and ARG 02/018 BB33 to V.L., and Martha Ferrario and R.A. respectively, further contributed with partial support. We are indebted to the anonymous reviewers for constructive inputs. This is INIDEP contribution No. 1689. References Acha, E.M., Mianzan, H., Guerrero, R., Favero, M., Bava, J., 2004. Marine fronts at the continental shelves of austral South America. Physical and ecological processes. Journal of Marine Systems 44, 83–105. Alemany, D., Acha, M.E., Iribarne, O., 2009. The relationship between marine fronts and fish diversity in the Patagonian Shelf Large Marine Ecosystem. Journal of Biogeography 36, 2111–2124. Almandoz, G.O., Ferrario, M.E., Ferreyra, G.A., Schloss, I.R., Esteves, J.L., Paparazzo, F.E., 2007. The genus Pseudo-nitzschia (Bacillariophyceae) in continental shelf waters of Argentina (Southwestern Atlantic Ocean, 38–55°S). Harmful Algae 6, 93–103. Angel, M.V., 1993. Biodiversity of the pelagic ocean. Conservation Biology 7, 760–772. Angel, M.V., 1997. Pelagic biodiversity. In: Ormond, R.F.G., Gage, J.D., Angel, M.V. (Eds.), Marine Biodiversity: Patterns and Processes. Cambridge University Press, Cambridge, pp. 35–68. Antacli, J.C., Hernández, D., Sabatini, M.E., 2010. Estimating copepods' abundance with paired nets: implications of mesh size for population studies. Journal of Sea Research 63, 71–77. Antacli, J.C., Sabatini, M., Akselman, R., Hernández, D., 2011. Seasonal variability of feeding and reproductive activity of the copepods Drepanopus forcipatus and Calanus australis in the Southern Patagonian Shelf: post-bloom versus earlybloom conditions. 5th International Zooplankton Production Symposium, Pucón (Chile), Book of Abstracts, S2-6932, p. 88. Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., Thingstad, F., 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10, 257–263. Bakun, A., 2006. Fronts and eddies as key structures in the habitat of marine fish larvae: opportunity, adaptive response and competitive advantage. Scientia Marina 70 (S2), 105–122. Barquero, S., Cabal, J.A., Anadon, R., Fernandez, E., Varela, M., Bode, A., 1998. Ingestion rates of phytoplankton by copepod size fractions on a bloom associated with an off-shelf front off NW Spain. Journal of Plankton Research 20, 957–972. Bastida, R., Rodríguez, D., 2003. In: Vázquez Mazzini (Ed.), Mamíferos marinos de Patagonia y Antártida. Buenos Aires, 208 pp. Belkin, I., Cornillon, P.C., Sherman, K., 2009. Fronts in large marine ecosystems. Progress in Oceanography 81, 223–236. Bianchi, A.A., Massonneau, M., Olivera, R.M., 1982. Análisis estadístico de las características T–S del sector austral de la plataforma continental argentina. Acta Oceanographica Argentina 3, 93–118.

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