The sub-Antarctic euthecosome pteropod, Limacina

ARTICLE IN PRESS Deep-Sea Research I 56 (2009) 582–598

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The sub-Antarctic euthecosome pteropod, Limacina retroversa: Distribution patterns and trophic role K.S. Bernard a,b,, P.W. Froneman a a b

Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa Elwandle Node, South African Environmental Observation Network, Grahamstown, South Africa

a r t i c l e i n f o

abstract

Article history: Received 9 November 2007 Received in revised form 13 November 2008 Accepted 21 November 2008 Available online 3 December 2008

Our understanding of the role that euthecosome pteropods play in the Southern Ocean is relatively limited. The aim of the present study was thus to examine the role of the sub-Antarctic species, Limacina retroversa, in the pelagic ecosystem of the Indian sector of the Polar Frontal Zone. Results from the study indicate that while L. retroversa might not dominate total mesozooplankton densities (the mesozooplankton community was always dominated by copepods, averaging 475% throughout the entire investigation), with an average contribution of only 5% to total mesozooplankton numbers, the species is capable of contributing substantially to total mesozooplankton grazing impact, outgrazing the dominant copepods (Calanus simillimuis, Ctenocalanus spp., Clausocalanus spp. and Oithona similis) 33% of the time. During the investigation, L. retroversa exhibited grazing impacts contributing to between 2% and 89% of the total per day. In addition to their exceptionally high grazing rates, our data suggest a coupling of L. retroversa densities to phytoplankton biomass. In fact, a significant decline in pteropod densities was recorded coinciding with extremely low phytoplankton concentrations. During the investigation the size structure of the pteropod community was predominantly made up of small- and medium-sized individuals; suggesting that spawning had taken place in summer during all 3 years. Although this trend was observed across all three surveys, the relative contributions of the three size classes varied significantly between the surveys, indicating a variable spawning period, similar to that observed in the northern hemisphere. In addition, reduced food availability during one of the surveys appeared to have resulted in delayed spawning as low relative abundances of small individuals and high relative abundances of large individuals were recorded during that survey. & 2008 Elsevier Ltd. All rights reserved.

Keywords: Euthecosome Thecosome Pteropod Limacina Retroversa Sub-Antarctic Polar Frontal Zone Southern Ocean Distribution patterns Grazing impact Trophic importance Population dynamics Ocean acidification

1. Introduction The role of the Southern Ocean in the global carbon cycle is, as yet, undefined (Caldeira and Duffy, 2000). Although extensive research has been carried out in the Southern Ocean, these studies have focussed, almost

Corresponding author at: Elwandle Node, South African Environmental Observation Network, Grahamstown, South Africa. Tel./fax: +2746 622 9899. E-mail address: [email protected] (K.S. Bernard).

0967-0637/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2008.11.007

entirely, on regions of high productivity, including the Marginal Ice Zone (Bathmann et al., 1993; Froneman et al., 1997), the neritic waters of Antarctica (Pakhomov and Perissinotto, 1997), the vicinity of the major oceanic fronts (Froneman and Perissinotto, 1996; Dubischar and Bathmann, 1997; Pakhomov and Perissinotto, 1997) and in the waters surrounding the Antarctic and sub-Antarctic islands (Perissinotto, 1992; Atkinson, 1994; Ward et al., 1995; Atkinson et al., 1996; Pakhomov et al., 1997). Apart from these regions of high productivity, the majority of the Southern Ocean is far less productive. The extreme environment of the Southern Ocean is the main cause of

ARTICLE IN PRESS K.S. Bernard, P.W. Froneman / Deep-Sea Research I 56 (2009) 582–598

low productivity; the region experiences very low temperatures, low to nil light availability for much of the year and persistent high winds, which reduce water column stability and generate a deep mixed layer, all of which are limiting factors for phytoplankton production (Laubscher et al., 1993; Dafner, 1997; Balarin, 1999; Froneman et al., 2001). Although the region exhibits high macronutrient concentrations, the low concentrations of trace metals, such as iron, contributes to the region’s high nutrient low chlorophyll (HNLC) status (Laubscher et al., 1993; Dafner, 1997; Lancelot et al., 2000; Bracher et al., 1999; Balarin, 1999; Froneman et al., 2001). One would therefore expect the region to be dominated by the microbial food web, or by microphagous meso- and macrozooplankton in the classical food web (Fortier et al., 1994; Le Fe`vre et al., 1998). A great deal of research has already been conducted on what have been termed ‘‘major’’ zooplankton grazers, including copepods, euphausiids and salps (Voronina, 1998). There are, however, a number of other zooplankton taxa that are recorded in high numbers in the Southern Ocean, yet have not been considered in terms of their grazing impact and contribution to biologically mediated carbon flux. Pteropods, although relatively understudied in the Southern Ocean, can account for a large proportion of total zooplankton numbers. For example, in the Polar Frontal Zone (PFZ) of the Southern Ocean the euthecosome pteropod, Limacina retroversa, is a relatively abundant member of the mesozooplankton community with average abundances ranging from 4 to 175 ind m3, which corresponds to between 4% and 17% of the total mesozooplankton densities (Perissinotto, 1992; Froneman and Pakhomov, 1998; Bernard and Froneman, 2002; Ward et al., 2003). Pteropods may also contribute substantially to total zooplankton biomass (Pakhomov and Froneman, 2004a). Pakhomov and Froneman (2004a) found that at the Spring Ice Edge (SIE) during December 1997–January 1998, the euthecosome pteropod, Clio sulcata, contributed 13% to total biomass. Because of their feeding mechanisms, euthecosome pteropods may be able to consume particles o5 mm in diameter (Perissinotto, 1992) and thus would be considered microphagous (Le Fe`vre et al., 1998). Euthecosomes feed typically on phytoplankton, but small zooplankton also form a substantial portion of their diets (Lalli and Gilmer, 1989). Studies on the grazing rates of some euthecosome pteropods suggest that they are capable of consuming large amounts of phytoplankton. During a survey conducted at the SIE over the period December 1997–January 1998, C. sulcata exhibited daily ingestion rates of up to 27 757 ng (pigm) ind1 day1, representing a contribution of as much as 53% of the total grazing impact in the region (Pakhomov and Froneman, 2004b). While data exist on their distribution patterns and, to some degree, grazing impact (see for example Perissinotto, 1992; Froneman and Pakhomov, 1998; Bernard and Froneman, 2002; Ward et al., 2003; Pakhomov and Froneman, 2004a, b; Bernard and Froneman, 2005) further investigations are required in order to better understand the role that euthecosome pteropods play in the region of the PFZ.

583

The aims of the present study were therefore: (1) to describe the distribution patterns and size class structure and (2) to examine the grazing impact of L. retroversa in the PFZ. For comparative purposes, the mesozooplankton community structure and the grazing impact of the numerically dominant copepods were also examined. 2. Materials and methods Mesozooplankton were collected during three research expeditions on board the MV SA Agulhas to the Indian sector of the PFZ during austral autumn. The expeditions were: (1) Marion Offshore Ecosystem Variability Survey II (MOEVS II, April 2002); (2) MOEVS IV (April 2004); and (3) MOEVS V (April 2005) (see Fig. 1). Sub-surface (200 m) temperatures were recorded throughout each survey with a Neil Brown MK III conductivity, temperature and depth (CTD) probe. Subsurface temperatures were used to detect major oceanic fronts: 6 1C for the Sub-Antarctic Front (SAF); 3.5 1C for the southern SAF (sSAF); and 2 1C for the Antarctic Polar Front (APF) (Ansorge et al., 2005). The following water masses were identified: (1) the southern Sub-Antarctic Zone (sSAZ) positioned between the SAF and sSAF; (2) the Polar Frontal Zone (PFZ) positioned between the sSAF and APF; and (3) the Antarctic Zone (AAZ) to the south of the APF (Fig. 2). Throughout the study, phytoplankton and mesozooplankton communities were compared between the water masses in order to determine whether they were a source of variability. In addition, inter-annual variability was compared not only for each survey as a whole, but also for each water mass, where possible. Note that, since the original aim was to examine the PFZ, either the sSAZ or the AAZ water masses were, during some surveys, sampled at only one station. Some statistical

Fig. 1. Voyage positions for Marion Offhsore Ecosystem Variability Survey (MOEVS) II, IV and V. Figure produced using the Ocean Data View package.

ARTICLE IN PRESS 584

K.S. Bernard, P.W. Froneman / Deep-Sea Research I 56 (2009) 582–598

Fig. 2. Station positions for Marion Offhsore Ecosystem Variability Survey (MOEVS) II (A), MOEVS IV (B) and MOEVS V (C) with sub-surface (200 m) temperatures. Figures produced using the Ocean Data View package.

comparisons could therefore not be made, for instance, inter-annual variability was not assessed for the sSAZ.

2.1. Phytoplankton biomass Total phytoplankton biomass was integrated over the top 100 m of the water column. Seawater samples, collected at five standard depths (0, 5, 20, 50 and 100 m) using a 12 8 L Niskin bottle rosette, were used to measure

chl-a concentrations by gently passing (o5 cm Hg) a 250 mL aliquot of seawater per depth through a Whatman GF/F filter. Total chl-a concentrations for each depth were measured fluorometrically, using a Turner Designs 10AU Fluorometer after 24 h of extraction at 20 1C in 90% acetone after the method of Holm-Hansen and Riemann (1978). Total chl-a concentrations were integrated over the top 100 m of the water column by trapezoidal integration. Integrated chl-a concentrations were expressed as mg m2. In addition, surface chl-a was size


fractionated during MOEVS IV and V by gently filtering 250 mL of seawater through a serial filtration unit, separating the phytoplankton into pico-(0.45–2.0 mm), nano-(2.0–20 mm) and micro-(420 mm) size fractions. Chl-a concentrations were measured fluorometrically as described above for each size fraction. 2.2. Mesozooplankton community During MOEVS II and V, mesozooplankton samples were collected by vertical tows using a WP-2 net fitted with a 200 mm mesh net and a 1.5 L cod-end. During MOEVS IV, mesozooplankton were collected at each station by oblique tows using a Bongo net fitted with 200 mm mesh nets. Tows were conducted to depths between 200 and 300 m. Samples were immediately fixed in 6% buffered formalin (hexamine). In the laboratory, sub-samples (1/64–1/32) from each station were sorted, identified and enumerated. The keys of Boltovskoy (1999) were used for zooplankton identification. For the purpose of the grazing study, mesozooplankton abundances were integrated over a standard depth of 100 m of the water column and were expressed as the number of individuals per square metre (ind m2). Additionally, the pteropod, L. retroversa, was separated into three size classes (after Dadon and de Cidre, 1992): (1) small/juveniles (o500 mm); (2) medium/males (500–1 500 mm); and (3) large/females (41500 mm) and counted. 2.3. Mesozooplankton ingestion rates and grazing impact The grazing impact of the dominant mesozooplankton taxa were measured using the gut fluorescence technique (Mackas and Bohrer, 1976). The taxa selected for the study included the four most abundant copepod species (C. simillimus, Clausocalanus spp., Ctenocalanus spp. and O. similis) (Fig. 3) as well as the euthecosome pteropod, L. retroversa. 30000 C.s. O.s. Cl Ct Other

Densities (ind. m-2)

25000 20000 15000

585

The estimation of the daily consumption of phytoplankton by the selected zooplankton requires the following variables: integrated gut pigment over 24 h (G, ng (pigm) ind1), gut evacuation rate (k, h1) and gut pigment destruction index (b0 , non-dimensional). Gut evacuation rates were determined for each of the four copepod species during MOEVS II and MOEVS IV, and only during MOEVS IV for L. retroversa. Due to size constraints, gut pigment destruction was only estimated for L. retroversa and was only determined during MOEVS IV, the value obtained for b0 during that survey was used to calculate ingestion rates for the pteropod during MOEVS II. An average value of 50% gut pigment destruction was assumed for the four copepod species (Perissinotto, 1992; Froneman et al., 2000). Due to time constraints at sea during MOEVS V, no ingestion rates were calculated on that survey. Instead, average individual daily ingestion rates for the four dominant copepods and L. retroversa were estimated for MOEVS V from linear regressions using integrated chl-a concentrations and individual ingestion rates measured for each taxon during MOEVS II and IV (Table 1). Although the results of the linear regression analyses were not statistically significant (P40.05 in all cases), the ingestion rates obtained for the taxa for MOEVS V from the regression equations are within the range of those from MOEVS II and IV. The use of linear regressions in this case to estimate ingestion rates is suitable given the constraints. Due to variability in the feeding activity of many zooplankton species as a result of diurnal migration patterns, gut pigment concentrations (G) were integrated over a 24-h period by trapezoidal integration. Mesozooplankton were collected at approximately 4 h intervals over 24 h. Samples collected were immediately anaesthetised in a solution of soda: seawater (1:5, v/v), after Morales et al. (1991), retained on a 200 mm mesh sieve and frozen at 20 1C in the dark for later analysis. In the laboratory, samples were thawed and individuals were quickly sorted under low light conditions using a Wild M5A Heerbrugg dissecting microscope, operated at 50 magnification. Once a sufficient number of individuals for each species were collected (40 O. similis; 20 C. simillimus, Clausocalanus spp. and Ctenocalanus spp.; 5–10 L. retroversa) they were placed into plastic centrifuge tubes (10 mL) with 8 mL of 90% acetone and extracted at 20 1C for 24 h. After centrifugation (5000 rpm), pigment content of the acetone extract was measured, before and after acidification using a Turner Designs 10AU Fluorometer (Mackas and Bohrer, 1976). Gut

10000 Table 1 Results of regression analyses used to estimate individual ingestion rates of the dominant copepods and the pteropod, Limacina retroversa, for the survey, MOEVS V.

5000 0 AAZ

PFZs Water Mass

SAZ

Fig. 3. Average contributions of dominant copepod taxa to total mesozooplankton densities in three different water masses. C.s. ¼ Calanus simillimus; O.s. ¼ Oithona similis; Cl ¼ Clausocalanus spp.; Ct ¼ Ctenocalanus spp.; Other ¼ remaining mesozooplankton; AAZ ¼ Antarctic Zone; PFZ ¼ Polar Frontal Zone; sSAZ ¼ southern Sub-Antarctic Zone. Error bars are standard deviation.

Taxon

Equation

Calanus simillimus Oithona similis Clausocalanus spp. Ctenocalanus spp. Limacina retroversa

y ¼ 705.66815.9723x y ¼ 166.4085+1.4623x y ¼ 439.821110.5155x y ¼ 276.90651.5299x y ¼ 4 231.95514.4327x

y ¼ individual daily ingestion rate; x ¼ integrated chl-a concentration.



pigment contents were calculated according to the method of Ba˚mstedt et al. (2000). It is important to note that only adult copepods were examined, while predominantly medium-sized individuals of L. retroversa were selected to estimate pteropod ingestion rates. The calculation of gut evacuation rate (k, h1) required that freshly caught zooplankton be gently placed into a 10 L plastic bucket filled with particle-free seawater (passed through a 0.2 mm filter) to which non-fluorescent charcoal powder had been added (Perissinotto, 1992). Experiments were carried out on deck at ambient seawater temperatures. Sub-samples were collected every 10 min for the first hour and every 20 min thereafter, and treated as described above. Total incubation time was 2 h. The gut evacuation rate was derived from the slope of the regression of the natural logarithm of gut pigments versus time (Dam and Peterson, 1988). The gut pigment destruction index (b0 ) of L. retroversa was determined using independent measurements of gut pigment loss. Active individuals were gently placed into a 10 L bucket of particle-free seawater (as described in the previous paragraph for gut evacuation rates) and allowed to empty their guts for 24 h. A two-compartment pigment budget approach was employed by comparing the decrease in pigment content in the grazing bottles with the increase in gut pigment levels of animals incubated in these bottles (Perissinotto, 1992). A total of ten replicates were prepared. Seawater with a natural phytoplankton assemblage was collected using a bucket over-board and poured into the 1 L incubation bottles. Prior to incubations, a 250 mL sub-sample of seawater was removed from each bottle to determine chl-a concentrations at the start of incubations. Only active L. retroversa individuals were placed into each incubation bottle (ten individuals per bottle). The animals were left to feed for 30 min to reduce the bottling effect and to minimise the production of faeces. At the end of the incubation period, only bottles with animals that were still active were used in the final stages of the experiment (only three out of the ten bottles had active pteropods during this experiment). The pteropods from each incubation bottle were removed and their gut pigments were determined fluorometrically. A 250 mL sub-sample of seawater was removed from each incubation bottle to determine final chl-a concentrations. Loss of pigment due to destruction was calculated using the following equation (Perissinotto, 1992): 0

b ð%Þ ¼ f½ðGt PbÞ=P 1g 100

(1)

where Gt is the gut content per individual, Pb the background fluorescence per individual and P the total amount of pigment ingested per individual (calculated from the difference between control and experimental water assemblages). Background fluorescence is determined by measuring the fluorescence of an individual after it has been starved for 24 h in particle-free water. Daily ingestion rates of selected zooplankton [I, ng (pigm) ind1 day1] were calculated using the following equation (Perissinotto, 1992): 0

I ¼ kG=ð1 b Þ

(2)

Taxon-specific grazing rates [mg (pigm) m2 day1] were calculated as the product of abundance and individual ingestion rates. Community grazing impact was then expressed as a percentage of the integrated phytoplankton biomass consumed per day. 2.4. Statistical analyses Statistical analyses were conducted using one- and two-way ANOVAs (StatSoft Inc., 2004 and SigmaStat, Version 8, 2002). Where appropriate, pairwise multiple comparison procedures were made using Student– Newman–Kuels Method or Dunn’s Method. All variables were log-transformed. Pearson’s correlation analysis was used to test for a relationship between surface phytoplankton biomass and L. retroversa densities. 3. Results 3.1. Phytoplankton biomass Integrated chl-a concentrations were significantly higher, at 15 mg m2, during MOEVS II than either of the following two surveys (Po0.001 in both cases; see Table 2). Chl-a concentrations during MOEVS V were the lowest recorded during the entire investigation, with an average of 8 mg m2 for that survey (P ¼ 0.037; see Table 2). Although trends highlighted in Table 2 suggest that integrated chl-a concentrations were elevated in the sSAZ during MOEVS II and were substantially lower in the PFZ and AAZ, insufficient data points for the sSAZ during that survey meant that the sSAZ could not be included in the statistical analysis. No significant variability in integrated phytoplankton biomass was observed between the water masses during any of the three surveys. During MOEVS IV, picophytoplankton dominated total surface chl-a concentrations, accounting for over 60% of the total phytoplankton biomass (Fig. 4A). Picophytoplankton contributed significantly more to total phytoplankton biomass during MOEVS IV than MOEVS V and this was largely observed in the sSAZ, where relative concentrations of this size fraction varied between 37% during MOEVS V and 70% during MOEVS IV (Po0.05 in both cases; Fig. 4A and B). During MOEVS V both the nano- and pico-fractions dominated, contributing approximately 42% and 55% to the total, respectively (Fig. 4B). Nanophytoplankton contributed significantly more to total phytoplankton biomass during MOEVS V than it did during MOEVS IV, this variability was observed in the AAZ and sSAZ (Po0.05 in both cases; Fig. 4A and B). On the whole, microphytoplankton contributed to an average of o10% during both surveys (Fig. 4A and B) and did not exhibit any inter-annual variability. No significant variability was observed between the water masses for any of the three size classes. 3.2. Mesozooplankton community structure Total mesozooplankton abundances ranged from a survey average of 16 177 ind m2 during MOEVS V to


120 Micro Nano Pico

100

%

80 60 40 20 0 AAZ

PFZ Water Mass

sSAZ

120 Micro Nano Pico

100 80 %

Values given are means per water mass per survey, with standard deviations in parenthesis. Water mass abbreviations: AAZ ¼ Antarctic Zone; PFZ ¼ Polar Frontal Zone; sSAZ ¼ southern Sub-Antarctic Zone.

8053.30 (6530.00) 63.09 (2.20) 8057.50 (9318.17) 79.23 (118.53) 29419.54 (25534.62) 18841.00 (17607.11) 4097.77 20500.41 29747.25 (16054.29) 4130.27 (3270.26) 22285.54 (16675.19) 475.08 (38.07) 2402.39 (2600.28) 124.71 1948.00 5743.06 (3739.94) 433.85 (392.41) 112.73 (125.76)

8.66 (1.96) 7.20 (1.96) 8.51 (0.52) 24133.92 (18069.43) 10269.82 (10864.80) 8885.46 (7000.25) 15.07 (3.58) 14.05 (2.85) 28.34 12.42 12.08 (4.88) 10.80 (3.69) 32810.49 (28427.22) 24429.84 (21761.93) 7155.29 30292.70 43850.90 (22403.77) 7373.56 (3206.14)

Integrated chl-a concentrations Total mesozooplankton abundance Dominant copepods abundance L. retroversa abundance

AAZ (n ¼ 10) PFZ (n ¼ 7) AAZ (n ¼ 1) AAZ (n ¼ 3)

PFZ (n ¼ 9)

sSAZ (n ¼ 1)

MOEVS IV MOEVS II

Table 2 Integrated chl-a concentrations (mg m2) and mesozooplankton abundances (ind m2) during MOEVS II, IV and V.

sSAZ (n ¼ 2)

MOEVS V

PFZ (n ¼ 11)

sSAZ (n ¼ 2)


60 40 20 0 AAZ

PFZ Water Mass

sSAZ

Fig. 4. Relative contribution of micro-, nano- and pico-size fractions to total phytoplankton biomass in three different water masses during the surveys: MOEVS IV (A) and MOEVS V (B).

35 200 ind m2 during MOEVS IV and did not vary significantly either with water mass or survey; however, there appeared to be a tendency for total densities in the sSAZ to be substantially lower than either the AAZ or the PFZ (Table 2). In addition, total mesozooplankton abundances appeared to be elevated during MOEVS IV, most notably in the PFZ (Table 2). During MOEVS IV, insufficient data points for the AAZ and sSAZ meant that statistical comparisons between these water masses and the PFZ could not be made. The copepods, C. simillimus, Clausocalanus spp., Ctenocalanus spp. and O. similis, were abundant throughout the entire investigation, dominating total mesozooplankton numbers (Fig. 3). Copepod densities were always significantly higher than those of L. retroversa (Po0.001; Table 2). Overall, the dominant copepods showed no significant variability either between the surveys or between the water masses (P40.05 in all



L. retroversa Copepods

Others

100

%

80

60

40

20

0 AAZ-II PFZ-II sSAZ-II AAZ-IV PFZ-IV sSAZ-IV AAZ-V PFZ-V sSAZ-V MOEVS II

MOEVS IV

MOEVS V

Fig. 5. Relative contribution of dominant copepods and Limacina retroversa to total mesozooplankton densities.

8 6 Log of L. retroversa

cases). Relative to L. retroversa, the copepods were more abundant in the AAZ, contributing an average of 90% to total mesozooplankton densities, when compared to the other water masses investigated during the study (Po0.05 in both cases; Fig. 5). The euthecosome pteropod, L. retroversa, was observed in significantly higher densities during MOEVS IV (Po0.001), where abundances averaged 4302 ind m2 than the low average abundances of 92 ind m2 recorded during MOEVS V (Table 2). This inter-annual variability was largely observed in the PFZ (Table 2). Significant variability in the densities of L. retroversa between the water masses was only observed during MOEVS IV, where values were greater in the PFZ, at an average of 5743 ind m2, than the sSAZ, where densities averaged 434 ind m2 (P ¼ 0.034; Table 2). The relative contribution of L. retroversa to total mesozooplankton abundances was greatest during MOEVS IV (Po0.001) and MOEVS II (Po0.001), the trend being apparent predominantly in the PFZ, where the species contributed an average of 14% and 11%, respectively, to the total (Fig. 5). Furthermore, during MOEVS IV, the relative densities of the pteropod were significantly higher in the PFZ than in the sSAZ (P ¼ 0.034). Results of a Pearson’s correlation analysis indicate that L. retroversa densities may be positively correlated to surface phytoplankton biomass (Fig. 6). Although this relationship is not particularly strong, it is significant (r2 ¼ 0.49; r ¼ 0.70; Po0.001). The size class structure of the L. retroversa populations varied between the surveys. During all three surveys, medium-sized individuals were most abundant (Po0.05 in all cases; Fig. 7), contributing an average of 54%

4 2 0 -2 -4 -4.0

-3.5

-3.0

-2.5 -2.0 -1.5 Log of chl-a

-1.0

-0.5

0.0

Fig. 6. Results of Pearson’s correlation analysis testing the relationship between phytoplankton biomass (chl-a) and Limacina retroversa abundances.

(average for entire investigation) to L. retroversa densities, compared with 23% and 12% average contributions made by small and large individuals, respectively. During MOEVS II, small individuals were equally as abundant as medium-sized individuals, both being more abundant than large individuals (Po0.05 in both cases; Fig. 7). The relative contribution of small individuals to total L. retroversa densities was greatest during MOEVS II and MOEVS V, with survey averages of 45% and 17%, respectively (Po0.001 in both cases; Fig. 7), while that of medium-sized individuals did not vary significantly


Small Medium

589

Large

100

80

%

60

40

20

0 AAZ-II PFZ-II sSAZ-II AAZ-IV PFZ-IV sSAZ-IV AAZ-V PFZ-V sSAZ-V MOEVS IV MOEVS II MOEVS V Fig. 7. Relative contribution of small, medium and large Limacina retroversa to total L. retroversa densities in three different water masses during the surveys: MOEVS II; MOEVS IV; and MOEVS V.

between the surveys. Large individuals made the greatest contribution to L. retroversa population structure during MOEVS V, where they contributed an average of 15% to the total, compared to MOEVS II and IV where large individuals contributed approximately 10% (Po0.05 in both cases; Fig. 7). Large individuals were the only size class to exhibit variability between water masses, contributing significantly more to population structure in the AAZ, with an average of 19%, when compared to either the PFZ or sSAZ, where the size class contributed o10% to the population (Po0.05 in both cases; Fig. 7).

3.3. Mesozooplankton grazing Analysis of diel variability of gut pigment contents indicated that, during MOEVS II, only the copepod, Clausocalanus spp. (Fig. 8) exhibited statistically significant differences in gut pigment content between day and night samples, with gut pigment concentrations being higher at night (P ¼ 0.036). The cyclopoid copepod, O. similis, and the calanoid copepods, C. simillimus and Ctenocalanus spp. (Fig. 8), showed no significant variation in gut pigment content over a 24-h period (P40.05 in all cases). Clausocalanus spp. exhibited similar trends in diel variability during MOEVS IV (Fig. 9), with significantly different gut pigment contents for day and night samples (Po0.001). In contrast to MOEVS II, C. simillimus and Ctenocalanus spp. showed significant diel variability in their gut pigments (Po0.001 in both cases). Gut pigments for taxa were elevated at night. O. similis did not exhibit

any significant diel variability in gut pigment contents during MOEVS IV (Fig. 9; P ¼ 0.719). In addition, the pteropod, L. retroversa, showed no significant variation in gut pigment concentrations between day and night samples (Fig. 9; P ¼ 0.661). Negative linear models provided the best fit for the decline in gut pigment contents during MOEVS II for Clausocalanus spp., Ctenocalanus spp. and O. similis, while a negative exponential model was most suitable to measure the decline in gut pigment contents for C. simillimus. During MOEVS IV, negative exponential models provided the best fit for the decline in gut pigment contents for all four copepod species and L. retroversa. Gut passage times for copepods were typically between 1 and 3 h and did not vary substantially between the years for each taxon, with the exception of Ctenocalanus spp., which showed a gut passage time of o1 h during MOEVS II (Table 3). On the other hand, L. retroversa exhibited a gut passage time of less than 1 h, which was observed during MOEVS IV (Table 3). Results of the two-compartmental approach for gut pigment destruction indicated that L. retroversa exhibited a mean pigment destruction of 58% (SD ¼ 7%). During MOEVS II, daily individual ingestion rates of the copepods were less than 330 ng (pigm) ind1 day1 (Table 3), while that of L. retroversa was an order of magnitude higher at 4147 ng (pigm) ind1 day1 (Table 3). During MOEVS IV, average daily individual ingestion rates of the copepods were more variable, but did not exceed 730 ng (pigm) ind1 day1 (Table 3). Average daily ingestion rates for L. retroversa, on the other hand, were similar to those observed during MOEVS II at



0.07

0.040 Calanus simillimus

Clausocalanus spp.

0.035 0.030

0.05

ug (pigm) ind-1

ug (pigm) ind-1

0.06

0.04 0.03 0.02

0.025 0.020 0.015 0.010

0.01

0.005

0.00

0.000 00:00

08:00

12:00

16:00

20:00

00:00

08:00

Time

20:00

16:00

20:00

0.016 Ctenocalanus spp.

0.014

0.014

Oithona similis

0.012

0.012

ug (pigm) ind-1

ug (pigm) ind-1

16:00

Time

0.018 0.016

12:00

0.010 0.008 0.006 0.004 0.002

0.010 0.008 0.006 0.004 0.002

0.000 -0.002

0.000

-0.004

-0.002 00:00

08:00

12:00

16:00

20:00

Time

00:00

08:00

12:00 Time

Fig. 8. Diel variability in gut pigment contents for the dominant copepod species (Calanus simillimus, Clausocalanus spp., Oithona similis and Ctenocalanus spp.) during Marion Offshore Ecosystem Variability Survey (MOEVS) II, April 2002. Thickened sections along x-axis represent times of darkness.

4129 ng (pigm) ind1 day1 (Table 3). Using the linear regression equations of ingestion rates versus integrated chl-a (taken from MOEVS II and IV), the estimated individual daily ingestion rates for the copepods during MOEVS V could be expected to range from 150 to approximately 580 ng (pigm) ind1 day1 (Table 3). In the same manner, average individual daily ingestion rate for L. retroversa during MOEVS V was estimated to be around 4200 ng (pigm) ind1 day1 (Table 3). Total grazing rates of the dominant mesozooplankton examined during the investigation exhibited significant variability between water masses during MOEVS IV only, where values were higher in the PFZ, at an average of 35 mg (pigm) m2 day1, than the sSAZ, where values average 4 mg (pigm) m2 day1 (P ¼ 0.001; Table 4). The variability in grazing rates between the AAZ and the PFZ could not statistically be compared as only one station had been occupied in the AAZ during MOEVS IV. Interannual variability was only apparent in the PFZ, with significantly elevated total grazing rates being recorded during MOEVS IV (Po0.001 in both cases; Table 4). Combined, the grazing rates of the dominant copepods ranged from an average of 4 mg (pigm) m2 day1 in the

sSAZ to approximately 8 mg (pigm) m2 day1 in the AAZ (Table 4). However, statistical analysis of variance did not reveal any significant differences in the grazing rates of copepods between any of the water masses encountered. Furthermore, no significant inter-annual variability was observed for copepod grazing rates (Table 4), and an average of 6 mg (pigm) m2 day1 was estimated during the entire investigation. L. retroversa showed significantly higher grazing rates during MOEVS II (P ¼ 0.014) and IV (Po0.001) than during MOEVS V (Table 4). This inter-annual variability was observed primarily in the PFZ (Po0.001 in both cases). Here, grazing rates of the pteropod varied from an average of 10 to approximately 24 mg (pigm) m2 day1 during MOEVS II and IV, respectively, while during MOEVS V grazing rates were significantly lower at mean of o1 mg (pigm) m2 day1 (Table 4). In addition, during MOEVS IV, L. retroversa grazing rates were significantly elevated from 2 mg (pigm) m2 in the sSAZ to 24 mg (pigm) m2 in the PFZ (P ¼ 0.032). Throughout the investigation, the total grazing impact by the dominant mesozooplankton grazers was observed to be significantly higher at 142% in the PFZ than in the


0.06

0.07 Calanus simillimus

0.05 0.04 0.03 0.02

0.00

0.03 0.02

0.00 00:00

08:00

12:00 Time

16:00

20:00

00:00

0.020 Ctenocalanus spp.

0.018

0.04

04:00

08:00 Time

16:00

20:00

08:00 Time

16:00

20:00

Oithona similis

0.016 ug (pigm) ind-1

ug (pigm) ind-1

0.04

0.01

0.01

0.05

Clausocalanus spp.

0.05 ug (pigm) ind-1

ug (pigm) ind-1

0.06

591

0.03 0.02 0.01

0.014 0.012 0.010 0.008 0.006 0.004

0.00

0.002 0.000 00:00

04:00

12:00

16:00

20:00

00:00

Time 0.12

04:00

Limacina retroversa

ug (pigm) ind-1

0.10 0.08 0.06 0.04 0.02 08:00

12:00

16:00 Time

20:00

Fig. 9. Diel variability in gut pigment contents for the dominant copepod species (Calanus simillimus, Clausocalanus spp, Oithona similis and Ctenocalanus spp.) and L. retroversa during Marion Offshore Ecosystem Variability Survey (MOEVS) IV, April 2004. Thickened sections along x-axis represent times of darkness.

sSAZ, where total grazing impacts averaged 48% (P ¼ 0.032). Significant inter-annual variability was only observed in the PFZ, where grazing impacts of 300% were greatest during MOEVS IV than either of the other two surveys (Po0.05 in both cases; Table 4). The combined grazing impacts of the dominant copepods did not show any significant variability between water masses (Table 4).

The copepods did, however, exert a significantly higher grazing impact during MOEVS V, with a survey average of 85%, than during MOEVS II, where the copepod grazing impact averaged 32% (P ¼ 0.027). The relative contribution of the dominant copepods to total grazing impact was greatest during MOEVS V, where values averaged 92% for that survey, as opposed to values of around 45% and 41%



Table 3 Gut evacuation rate constants (k, h1); gut passage time (1/k, h); and average daily ingestion rates (I, ng (pigm) ind1 day1) of selected mesozooplankton. Taxon

Gut evacuation rate (k, h1)

Gut passage time (1/k, h)

Average daily ingestion rate (I, ng (pigm) ind1 day1)

Survey

1.33

0.75

4146.51 (1 296.82) 4128.68 (892.23) 4196.88 (8.56)

MOEVS II MOEVS IV MOEVS V

C. simillimus

0.32 0.50

3.15 2.00

321.95 (108.10) 728.36 (644.03) 579.28 (30.84)


Clausocalanus spp.

0.44 0.35

2.25 2.86

180.05 (44.00) 454.16 (194.97) 356.61 (20.30)


Ctenocalanus spp.

1.43 0.34

0.70 2.94

237.30 (103.35) 265.37 (147.50) 264.80 (2.95)


O. similis

0.77 0.57

1.30 1.75

182.10 (68.41) 159.32 (84.98) 177.98 (2.82)


L. retroversa

Standard deviation in parenthesis.

recorded during MOEVS II and IV, respectively (Po0.05 in both cases; Fig. 10). This inter-annual variability was only significant in the PFZ. Inter-annual variability of L. retroversa grazing impacts was observed only in the PFZ, where significantly higher grazing impacts of approximately 185% and 74% were recorded during MOEVS IV and MOEVS II, respectively, as opposed to the grazing impacts of 6% observed during MOEVS V (Po0.05 in both cases; Table 4). Throughout the investigation, L. retroversa grazing impacts were higher in the PFZ, where values averaged 75%, compared to approximately 10% in the sSAZ (P ¼ 0.019; see Table 4). The contribution of L. retroversa to total grazing impact was significantly higher during MOEVS II (Po0.001) with an average of 55% and MOEVS IV (Po0.001) where grazing impacts averaged 60%, when compared to MOEVS V, where an average of 8% was estimated (Fig. 10). Inter-annual variability was largely observed in the PFZ, where the contribution of L. retroversa to total grazing impacts during MOEVS II and IV averaged 64% compared to 8% recorded during MOEVS V (Po0.001 in both cases; Fig. 10).

200 m depth), which was most likely caused by topographic steering through the Andrew Bain Fracture Zone on the South-West Indian Ridge (Froneman et al., 2002; Ansorge and Lutjeharms, 2005). During MOEVS IV, an intense frontal feature was observed flowing in a northward direction between 30.51 and 31.51E and represented the coincidence of three fronts: the SAF, sSAF and APF (Ansorge et al., 2004). As for MOEVS II, the northward movement and near-joining of these fronts was probably due to the interaction of the Antarctic Circumpolar Current (ACC) and the Andrew Bain Fracture Zone (Ansorge and Lutjeharms, 2005). A cold core eddy of Antarctic Zone (AAZ) origin was the main focus of the investigation during MOEVS V (see also the study by Bernard et al., 2007). The eddy edge was identified using the 2 1C sub-surface (200 m) isotherm, which is typically used to locate the APF (Ansorge et al., 2005). The waters surrounding the eddy were typical of the PFZ. The sSAF, and consequently the sSAZ, was also present in the survey region. The physical nature of the eddy has been described in detail in another paper by Ansorge et al. (2006).

4. Discussion 4.2. Phytoplankton biomass 4.1. Brief description of environmental conditions encountered during the investigation MOEVS II was occupied in the vicinity of the APF (2 1C at 200 m depth), which lay between 50.51 and 51.251S. At 30.51E, a tongue of warmer water intruded to about 50.251S, representing a meander in the sSAF (3.5 1C at

Integrated phytoplankton biomass during MOEVS II and IV was typical for the region and season (BradfordGrieve et al., 1998; Froneman et al., 2001). Integrated phytoplankton biomass during MOEVS V, on the other hand, was substantially lower than expected for the region, which could be the result of grazing pressure by

ARTICLE IN PRESS (6.04) (6.04) (0.01) (76.14) (75.84) (0.30) 6.88 6.62 0.26 83.21 80.09 3.12 (3.87) (3.47) (0.50) (83.84) (75.05) (10.19) 4.16 3.83 0.33 71.16 65.65 5.51 (8.11) (7.68) (0.53) (92.66) (88.41) (6.35) 9.12 8.65 0.47 112.35 106.50 5.85 (0.13) (1.75) (1.62) (10.92) (11.03) (21.95) 3.63 1.84 1.79 35.51 15.18 20.33

4.3. Mesozooplankton community: emphasis on Limacina retroversa

Values given are means per water mass per survey, with standard deviations in parenthesis.

14.96 6.92 8.04 120.45 55.69 64.76 14.29 4.33 9.96 104.27 30.63 73.64 (4.64) (4.73) (0.16) (27.02) (26.86) (4.96) 8.56 6.59 1.97 57.81 43.96 13.85 Total mesozooplankton grazing rates Dominant copepods grazing rates L. retroversa grazing rates Total mesozooplankton grazing impacts Dominant copepods grazing impacts L. retroversa grazing impacts

PFZ (n ¼ 9)

(13.55) (4.14) (10.78) (106.78) (27.15) (89.24)

1.29 0.77 0.52 4.54 2.72 1.82

AAZ (n ¼ 1) AAZ (n ¼ 3)

sSAZ (n ¼ 1)

MOEVS IV MOEVS II

Table 4 Mesozooplankton grazing rates (mg pigm m2 day1) and grazing impacts (%) during MOEVS II, IV and V.

593

zooplankton (see below). The elevated phytoplankton biomass in the sSAZ during MOEVS II is likely due to a single station, where the integrated chl-a concentration recorded was almost 30 mg m2. However, it must be pointed out that only a single station was occupied in the sSAZ during MOEVS II, it is therefore not clear whether this result is representative of the water mass or simply an outlier. For the remainder of the investigation, no other variability in phytoplankton biomass was observed between the water masses. During MOEVS IV total phytoplankton biomass was dominated by the picophytoplankton fraction, while both pico- and nanophytoplankton dominated during MOEVS V. The predominance of small phytoplankton is a common feature for the region (Laubscher et al., 1993; Xiuren et al., 1996; Froneman et al., 2001) and is the result of a combination of factors including low light availability, low water column stability (i.e. deep mixed-layer depths), low surface temperatures and low trace metal (particularly iron) availability (Laubscher et al., 1993; Dafner, 1997; Lancelot et al., 2000; Bracher et al., 1999; Balarin, 1999; Froneman et al., 2001). Small phytoplankton (o20 mm) are better able to grow and reproduce in these conditions due to their small surface area:volume ratio (Fogg, 1991).

(15.10) (7.44) (15.25) (218.81) (154.64) (108.34) 34.63 11.02 23.61 300.54 115.95 184.59

AAZ (n ¼ 10) sSAZ (n ¼ 2) PFZ (n ¼ 7)

MOEVS V

PFZ (n ¼ 11)

sSAZ (n ¼ 2)


Total mesozooplankton abundances recorded during the three surveys ranged between 1676 ind m2 (Station 291, MOEVS V) and 87 083 ind m2 (Station 228, MOEVS IV). These values are typical for the Southern Ocean (Perissinotto, 1992; Pakhomov and Perissinotto, 1997; Pakhomov et al., 1997; Froneman and Pakhomov, 1998; Froneman et al., 2000; Pakhomov and Froneman, 2004b). For example, during winter, in the region of the Subtropical Convergence, total mesozooplankton abundances ranged from 1446 to 25 333 ind m2 (Pakhomov and Perissinotto, 1997), while at South Georgia, during austral summer, total mesozooplankton numbers ranged between 15 698 and 46 907 ind m2 (Pakhomov et al., 1997). Furthermore, during the present investigation, total mesozooplankton densities were consistently higher south of the sSAF, in the colder, more productive waters of the AAZ and the PFZ. These findings are similar to those of a study conducted by Ward et al. (2003) across the Antarctic Circumpolar Current to the north of South Georgia. During that study, conducted over four consecutive summers, the PFZ was characterised by the highest overall mesozooplankton abundances, while the SAZ exhibited the lowest total mesozooplankton abundances (Ward et al., 2003). As is typical of the Southern Ocean, copepods numerically dominated the mesozooplankton counts throughout the three surveys, accounting for up to 96% of all mesozooplankton counted (Hopkins, 1985; Conover and Huntley, 1991; Perissinotto, 1992; Atkinson and Shreeve, 1995; Atkinson, 1996; Atkinson et al., 1996; Pakhomov et al., 2000; Bernard and Froneman, 2002; Ward et al., 2003; Pakhomov and Froneman, 2004a). The copepod community consisted primarily of C. simillimus, Clausocalanus spp.,



L. retroversa

Copepods

100

80

%

60

40

20

0 AAZ-II

PFZ-II sSAZ-II AAZ-IV PFZ-IV sSAZ-IV AAZ-V MOEVS II

MOEVS IV

PFZ-V sSAZ-V MOEVS V

Fig. 10. Relative contribution of dominant copepods and Limacina retroversa to total grazing impact. Values presented are averages for three different water masses during the surveys: MOEVS II, MOEVS IV and MOEVS V.

Ctenocalanus spp. and O. similis. Although the euthecosome pteropod, L. retroversa, was significantly less abundant than the dominant copepods, it was recorded in almost all samples in densities that varied from 0 to 10 741.99 ind m2, contributing between 0% and 30% to total mesozooplankton abundances. L. retroversa generally contributed approximately 10% to total mesozooplankton numbers during MOEVS II and IV, but only an average of o1% during MOEVS V. In addition, L. retroversa made the greatest contribution to total mesozooplankton abundances in the PFZ, and to some extent, the AAZ. The high densities of the pteropod in the PFZ and AAZ is to be expected since it is a sub-Antarctic species and would not typically occur in the warmer waters north of the sSAF (Boltovskoy, 1999). The occurrence of the species south of the APF is possibly due to cross-frontal mixing that is known to occur frequently as a result of eddy formation in this region of the Southern Ocean (Ansorge and Lutjeharms, 2005). Pearson’s correlation analysis results from the present investigation indicate a coupling between L. retroversa densities and surface chl-a concentrations (see Results section). Indeed, Seibel and Dierssen (2003) suggest that L. helicina (the Arctic/Antarctic species) may be strongly affected by regional phytoplankton concentrations. Similarly, Kobayashi (1974) reported that, in the Arctic, the availability of food is very important for Spiratella (‘‘Limacina’’) helicina as the pteropod requires a continuous source of nutritive particulate organic matter in order to sustain the growth cycle. The elevated densities of L. retroversa during MOEVS II and IV may therefore be due to the possible dependency of L. retroversa on phytoplankton and the fact that integrated phytoplankton biomasses observed during those surveys were signifi-

cantly higher than during MOEVS V. It is therefore likely that the low numbers of L. retroversa observed during MOEVS V can be attributed to the low chl-a concentrations recorded during that survey. The size class structure of L. retroversa varied significantly between the years but generally not between water masses, with the exception of large individuals, which were recorded in greater densities in the AAZ than in the PFZ (see Results section). This inter-annual variability in size class structure suggests variable spawning times. For instance, the percentage contribution of small individuals to total pteropod numbers was significantly lower during MOEVS IV than either MOEVS II or V. This may either indicate regional delayed spawning or early season spawning during that survey. Although the densities of medium-sized pteropods did not vary significantly between the surveys, observations of the data suggest that during MOEVS IV, medium-sized individuals contributed relatively more to the composition of L. retroversa than during the other two surveys. This suggests that, during that survey, spawning may have taken place earlier in the season, particularly since the relative contribution of large individuals is low. On the other hand, the relatively similar contributions to total L. retroversa densities by all three size classes during MOEVS V suggest that, while some spawning might have occurred earlier in the season, further spawning appeared to have been delayed. This might have been caused by low food availability during MOEVS V. In fact, relatively short delays in food supply have been shown to effect reproductive success, resulting in failed metamorphosis of some larval zooplankton (Ross and Quetin, 1989). Furthermore, large individuals of L. retroversa contributed significantly more to total


pteropod numbers during MOEVS V than during either of the other two surveys, reinforcing the hypothesis that spawning had been delayed. Typically, most adult females die after spawning (Kobayashi, 1974; Gannefors et al., 2005). The presence of high numbers of large individuals of L. retroversa during that survey, therefore suggests that they had not yet spawned. The overall predominance of medium and small individuals during the three surveys suggests that the life cycle of L. retroversa in the subAntarctic is similar to that of L. helicina in the Arctic (Kobayashi, 1974; Gannefors et al., 2005). For L. helicina, spawning occurs primarily during summer, peaking in late summer, with some spawning still occurring until late autumn (Gannefors et al., 2005). Similarly, the results of the present investigation suggest that spawning had occurred during early to late summer in all 3 years.

4.4. Mesozooplankton grazing: emphasis on the trophic role of L. retroversa Diel variability in gut pigment content was only observed for one of the calanoid copepods, Clausocalanus spp., during MOEVS II and for all three calanoid copepods (C. simillimus, Clausocalanus spp. and Ctenocalanus spp.) during MOEVS IV. These results reflect the diel vertical migration patterns of the species commonly reported in other studies in the region (Atkinson et al., 1992a, b; Perissinotto, 1992). The absence of any significant diel variability in gut pigment contents for the cyclopoid copepod, O. similis, and the pteropod, L. retroversa, during the investigation can thus likely be ascribed to these species exhibiting less pronounced diel vertical migrations. It is worth noting that Atkinson et al. (1996) reported that both O. similis and an unidentified pteropod remained in the upper 40 m of the water column during both the day and night. While data for gut evacuation rates of copepods are numerous in the literature (Perissinotto, 1992; Atkinson, 1996; Atkinson et al., 1996; Pakhomov and Perissinotto, 1997; Pakhomov et al., 1997; Froneman et al., 2000; Pakhomov and Froneman, 2004b), few reports on the gut evacuation rate of Limacina spp. (Perissinotto, 1992; Pakhomov and Perissinotto, 1997). Pakhomov and Perissinotto (1997) found that Limacina spp. exhibited a gut evacuation rate of o0.5 h1 in the Subtropical Convergence during austral winter. The gut evacuation rate reported in the present study, 1.33 h1, is substantially more rapid with the evacuation of the gut contents being completed in just over 45 min. The discrepancy between the two values may be due to spatial or temporal differences between the studies or simply due to the fact that different species may exhibit varying gut evacuation rates. Indeed, it is well documented that the gut passage time and pigment destruction in copepods may reflect variable food concentrations (Wang and Conover, 1986; Dagg and Walser, 1987), seawater temperature (Dam and Peterson, 1988) and feeding history (Head, 1988). Perissinotto (1992) measured gut evacuation rates for Limacina sp. in the vicinity of the Prince Edward

595

Archipelago, PFZ, during austral autumn and recorded a value of 0.98 h1, which is closer to the value that was recorded during the present study (1.33 h1). It is likely that the differences between the gut evacuation rates may be the result of variable food concentrations and/or the availability of preferentially sized food particles during the different studies (Wang and Conover, 1986; Dagg and Walser, 1987; Pasternak, 1994). Perissinotto (1992) recorded chl-a concentrations that were much higher than those measured during the present study. Furthermore, during the study conducted by Perissinotto (1992), nano(2.0–20.0 mm) and microphytoplankton (420.0 mm) composed up to 86% of the total pigment. In contrast, the phytoplankton biomass during the present study was almost entirely dominated by pico-o2.0 mm) and nanophytoplankton. Perissinotto (1992) noted that Limacina sp. preferentially grazed on particles o5 mm, and it was suggested that the ingestion of larger cells might be limited by the dimensions of the ciliated grooves through which the food enters the mouth. The predominance of unpalatable food particles during the study by Perissinotto (1992) might have resulted in reduced assimilation efficiencies and thus reduced gut evacuation times. Unfortunately, as far as we are aware, no data exist on the assimilation efficiencies of L. retroversa. The gut pigment destruction rate of 58% for the pteropod, L. retroversa, appears to be the first estimate made for this species. Perissinotto (1992) assumed a gut pigment destruction rate of 60% for L. retroversa, which was obtained by averaging the destruction rates, estimated for large copepods and euphausiids. Daily individual ingestion rates of the copepods examined during the present study are similar to those reported during previous investigations in the Southern Ocean (Perissinotto, 1992; Atkinson, 1996; Atkinson et al., 1996; Pakhomov and Perissinotto, 1997; Pakhomov et al., 1997; Froneman et al., 2000; Pakhomov and Froneman, 2004b). L. retroversa, however, exhibited a substantially greater daily individual ingestion rate during the present study than any other previous reports (Perissinotto, 1992; Pakhomov and Perissinotto, 1997; Pakhomov and Froneman, 2004b). For example, during austral autumn in the vicinity of the Prince Edward Archipelago in the PFZ, Limacina sp. exhibited daily ingestion rates an order of magnitude less than those of the present study (Perissinotto, 1992). However, as discussed in the previous paragraph, the phytoplankton community during that study was comprised largely of phytoplankton that were 45 mm (micro- and nanophytoplankton) and were thus likely to be less palatable to the pteropod (Perissinotto, 1992). The elevated ingestion rates obtained for the pteropod during the present study might therefore be the result of an abundance of preferentially sized food particles. Total zooplankton grazing rates during previous investigations in the Southern Ocean have been highly variable, ranging from o1 to 72 mg (pigm) m2 day1 (Perissinotto, 1992; Froneman et al., 1997; Pakhomov et al., 1997; Pakhomov and Perissinotto, 1997; Froneman et al., 2000; Li et al., 2001; Pakhomov and Froneman, 2004b). Average zooplankton grazing rates during the



present study can thus be considered as typical for the region, ranging between 0.7 mg (pigm) m2 day1 (Station 291, MOEVS V) and 52 mg (pigm) m2 day1 (Station 229, MOEVS IV). Total mesozooplankton grazing rates were elevated in the PFZ during MOEVS IV. Not only were the grazing rates observed in the PFZ greater than the surrounding water masses, but they were significantly higher than those recorded in the same water mass during MOEVS II and V. Although phytoplankton biomass recorded during MOEVS IV was lower than that observed during MOEVS II, the occurrence of microphytoplankton in the samples and the predominance of picophytoplankton suggest that the area may either have experienced bloom conditions prior to the survey and was subsequently in a state of nutrient depletion (Froneman et al., 2001) or that the phytoplankton community had been controlled by zooplankton grazing. Indeed, the strong frontal feature created by the near-joining of the APF, sSAF and SAF during MOEVS IV would likely have resulted in elevated primary production. Unfortunately, no primary productivity measurements were taken during any of the surveys to verify this statement. The elevated mesozooplankton grazing rates observed during MOEVS IV may therefore partially explain the lower phytoplankton biomass recorded during that survey. L. retroversa was primarily responsible for the extremely high grazing rates exhibited in the PFZ during MOEVS IV, with grazing rates reaching up to 44 mg (pigm) m2 day1 (Station 229); double that of the dominant copepods combined. Furthermore, the grazing impact of L. retroversa recorded in the PFZ during MOEVS IV was higher than that recorded in either of the other water masses or surveys. Grazing rates of L. retroversa were also significantly raised in the PFZ during MOEVS II, where phytoplankton biomass was enhanced. During both MOEVS II and IV, L. retroversa contributed substantially more (significantly more during MOEVS IV) to total grazing impact than the dominant copepods, despite the fact that the pteropods were recorded in significantly lower abundances than the dominant copepods. On the other hand, during MOEVS V, when densities of the pteropod were significantly lower than during the previous two surveys, L. retroversa made little contribution to overall grazing impact and exhibited reduced grazing rates. Throughout the investigation L. retroversa grazing rates and grazing impact was greater in the PFZ than in either of the other two water masses. This stands to reason, as the PFZ is the preferred water mass of L. retroversa (Boltovskoy, 1999). Total zooplankton grazing impact ranged from 5% to 768% of the available phytoplankton standing stock throughout the three surveys combined, with averages of 86%, 230% and 90% for MOEVS II, IV and V, respectively. These values are the highest reported for the Southern Ocean (Perissinotto, 1992; Froneman et al., 1997; Pakhomov et al., 1997; Pakhomov and Perissinotto, 1997; Li et al., 2001; Urban-Rich et al., 2001; Froneman et al., 2000; Pakhomov and Froneman, 2004b). However, in most previous investigations the grazing impact of the pteropod, L. retroversa, was not considered (Froneman

et al., 1997, 2000; Li et al., 2001; Urban-Rich et al., 2001). If we ignore the impact of L. retroversa in the present study, then the average daily grazing impact of the numerically dominant mesozooplankton, the four dominant copepods, is equivalent to 39%, 90% and 90% of the phytoplankton biomass for MOEVS II, IV and V, respectively. These values are now in line with those reported in previous investigations (Perissinotto, 1992; Froneman et al., 1997; Pakhomov et al., 1997; Pakhomov and Perissinotto, 1997; Li et al., 2001; Urban-Rich et al., 2001; Froneman et al., 2000; Pakhomov and Froneman, 2004b). This result highlights the importance of studying all major zooplankton taxa, and not only those that are most abundant. As previously mentioned, no primary productivity measurements were made during the investigation, we were therefore unable to estimate the impact that mesozooplankton grazing would have on phytoplankton production. It should be noted that the present study does not consider the potential influence of biological interactions (e.g. interspecific competition and predation) in mediating the grazing impact of the herbivorous zooplankton. For example, a trophic cascading study, conducted by Froneman and Bernard (2004) in the PFZ, demonstrated that the addition of carnivorous zooplankton to incubation bottles coincided with a decreased impact of the herbivorous zooplankton on the phytoplankton standing stocks.

5. Concluding remarks 5.1. The role of euthecosome pteropods in the sub-Antarctic region of the Southern Ocean Results of the present study highlight the role that the euthecosome pteropod, L. retroversa, plays in the subAntarctic ecosystem in the Indian sector of the Southern Ocean, particularly in the PFZ. L. retroversa can, at times, contribute substantially to total mesozooplankton numbers and can be considered a major grazer in the zooplankton community. L. retroversa employs a similar feeding mechanism to the tunicate, Salpa thompsoni, the use of mucous mesh to trap food particles. In this way, L. retroversa is capable of consuming large quantities of phytoplankton, as well as microzooplankton. Furthermore, L. retroversa appears to be heavily reliant on food availability. Thus, not only does the species show extremely high grazing rates but they seem to aggregate in areas of high phytoplankton biomass. Euthecosome pteropods enhance the sequestration of carbon to the sea floor, through the sinking of large faecal pellets and abandoned mucous webs; and, in death, the mass sedimentation of empty shells (Lalli and Gilmer, 1989; Meinecke and Wefer, 1990; Bathmann et al., 1991; Noji et al., 1997; Collier et al., 2000; Gardner et al., 2000; Yoon et al., 2001; Accornero et al., 2003). In regions where L. retroversa contributes significantly to total mesozooplankton grazing impact, they are therefore likely to contribute substantially to carbon flux and sequestration. Furthermore, euthecosome pteropods contribute to the transfer of organic carbon through the pelagic food web.


In particular, Limacina spp. are the exclusive prey items of the gymnosome pteropod, Clione limacina (Lalli and Gilmer, 1989). 5.2. Potential implications of ocean acidifcation on Southern Ocean pelagic ecosystems It has been predicted that continued anthropogenic emissions of CO2 will result in an increase in the acidity of the surface waters of the world’s high-latitude oceans, with a corresponding decrease in the calcium carbonate (CaCO3) saturation depth (Caldeira and Wickett, 2003; Feely et al., 2004; Orr et al., 2005). If the acidity of highlatitude oceans increases and the waters become undersaturated with regard to CaCO3, then it is unlikely that euthecosome pteropods in the high-latitude regions will survive (Feely et al., 2004; Orr et al., 2005). This might have implications for the entire pelagic ecosystem of the high latitudes, the extent of which is yet to be determined with further research.

Acknowledgements We would like to thank the South African Departments of Environmental Affairs & Tourism and Science & Technology, as well as the National Research Foundation, for providing funding for this research through the South African National Antarctic Programme. We are grateful to the Department of Zoology and Entomology, Rhodes University, for providing the necessary space and equipment to carry out this research. An anonymous reviewer provided valuable input to the manuscript. Thanks are also due to the various captains and crew members of the MV SA Agulhas during voyages to the Southern Ocean and to all of the ship-based scientific teams from the three surveys. References Accornero, A., Manno, C., Esposito, F., Gambi, M.C., 2003. The vertical flux of particulate matter in the polynya of Terra Nova Bay. Part II. Biological components. Antarctic Science 15, 175–188. Ansorge, I.J., Lutjeharms, J.R.E., 2005. Direct observations of eddy turbulence at a ridge in the Southern Ocean. Geophysical Research Letters 32, L14603. Ansorge, I.J., Froneman, P.W., Bernard, K.S., Bernard, A., Lange, L., Lukaćˇ, D., Backeberg, B., Blake, J., Bland, S., Burls, N., Davies-Coleman, M., Gerber, R., Gildenhuys, S., Hayes-Foley, P., Ludford, A., Manzoni, T., Robertson, E., Southey, D., Swart, S., Van Rensburg, D., Wynne, S., Lutjeharms, J.R.E., 2004. Further investigations on the sources of mesoscale variability in the Antarctic Circumpolar Current at the South-West Indian Ridge. South African Journal of Science 100, 319–323. Ansorge, I.J., Speich, S., Lutjeharms, J.R.E., Go¨ni, G.J., W. de Rautenbach, C.J., Froneman, P.W., Rounault, M., Garzoli, S., 2005. Monitoring the oceanic flow between Africa and Antarctica: report of the first GoodHope cruise. South African Journal of Science 101, 29–35. Ansorge, I.J., Lutjeharms, J.R.E., Swart, N., Durgadoo, J.V., 2006. Observational evidence of a cross frontal heat pump in the Southern Ocean. Geophysical Research Letters 33, L19601. Atkinson, A., 1994. Diets and feeding selectivity among the epipelagic copepod community near South Georgia in summer. Polar Biology 14, 551–560. Atkinson, A., 1996. Subantarctic copepods in an oceanic, low chlorophyll environment: ciliate predation, food selectivity and

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