Spatio-temporal variability of small copepods (especially Oithona plumifera) in shallow nearshore waters off the south coast of South Africa

Estuarine, Coastal and Shelf Science 72 (2007) 711e720 www.elsevier.com/locate/ecss

Spatio-temporal variability of small copepods (especially Oithona plumifera) in shallow nearshore waters off the south coast of South Africa Francesca Porri*, Christopher D. McQuaid, William P. Froneman Coastal Research Group, Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, Eastern Cape, South Africa Received 8 March 2006; accepted 11 December 2006 Available online 7 February 2007

Abstract Although small copepods are one of the main dietary sources for many commercially important fish, their role in the pelagic trophic dynamics has traditionally been underestimated due to the methodology commonly used in plankton sampling. Temporal variation in abundance of adults and nauplii of small copepods (particularly Oithona plumifera) in nearshore waters on the south coast of South Africa was investigated fortnightly over 14 months at site (km) and location (100 m) scales. Sampling was within <500 m of the shore, where depth was ca. 10 m, using vertical hauls of an 80-mm mesh plankton net from 1 m above the seabed to the surface. Twenty-seven adult copepod taxa were recorded, but Oithona spp. was consistently the most abundant. Taxon richness was 7e19 on each sampling occasion. There was strong temporal variation (Oithona varied between 0 and 2300 m3), but much of this was short-term variability (e.g. between consecutive sampling sessions), with no seasonality or other long-term discernable patterns. There were periods of consistently low numbers, but very high numbers often followed samples with low abundances. Nor was there spatial structure at the location scale, though numbers differed between sites. Despite considerable variability at the location scale within sites, Kenton consistently showed higher densities than High Rocks. Separate analyses, with Bonferroni adjustment, showed that this difference was significant on eight out of 21 occasions for Oithona, six for other pelagic copepods and three for nauplii. This suggests that hydrodynamics favour aggregation of plankton at Kenton. A high degree of short-term variability, with a tendency for aggregation of small zooplankton at certain sites has implications for both pelagic processes and food-web links between the benthic and pelagic environments. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: spatio-temporal variability; small copepods; Oithona plumifera; Oithona spp; zooplankton; patchiness; inshore pelagic food web; South Africa; Kenton-on-Sea

1. Introduction Copepods are among the most abundant components of coastal and oceanic zooplankton assemblages (Huggett and Richardson, 2000; Calbet et al., 2001; Peterson and Keister, 2002; Albaina and Irigoien, 2004), and variability in their abundance in time and space is important to the dynamics of marine food webs. In particular, copepods are important

* Corresponding author. E-mail address: [email protected] (F. Porri). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2006.12.006

food sources for larger predators, including fish larvae (Sa´nchez-Velasco, 1998; Hsieh and Chiu, 2002), gelatinous siphonophores (Thibault-Botha et al., 2004), chaetognaths (Saito and Kiørboe, 2001) and squid paralarvae (Roberts, 2005). As well as their importance as food for larger predators, copepods can themselves have important effects on lower trophic levels and the spatial and temporal variabilities of copepod abundance can also help clarify movement of water masses and zooplankton patchiness (Fennel, 2001; Verheye et al., 2001). Of the many studies of spatial and temporal patterns in zooplankton communities, very few have concentrated on

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small-sized copepods (Chisholm and Roff, 1990; Fransz and Gonzalez, 1995; Webber and Roff, 1995; Calbet et al., 2001; Hansen et al., 2004). Amongst small copepods, the cyclopoid Oithona is a key element and can be regarded as the most abundant genus in the zooplankton community (Omori et al., 1995; Soussi et al., 2000; Keister and Peterson, 2003; Vieira et al., 2003). Oithona has a very wide distribution and occurs in almost any marine environment (Paffenho¨fer, 1993), from estuaries (Gaughan and Potter, 1995) to open waters, from Arctic (Falk-Petersen et al., 1999; Lischka and Hagen, 2005) and Antarctic (Fransz and Gonzalez, 1995) to Mediterranean (Mazzocchi and Ribera d’Alcala’, 1995) and tropical and sub-tropical waters (Paffenho¨fer, 1998). This wide distribution is partly due to the fact that some species have eurysaline (Torres-Sorando et al., 2003; Hansen et al., 2004), and eurythermal characteristics (Turner, 2004), in addition to low respiration and metabolic rates (Paffenho¨fer, 1993). Species in the genus Oithona have a wide range of diets. Some species are primary consumers of phytoplankton, while others are coprophagous, feeding on faecal pellets and helping to remove faecal material from the euphotic zone (Gonza´lez and Smetacek, 1994). Coprophagy also helps to explain the wide distribution of Oithona, as faecal pellets are a universal source of food (Gonza´lez and Smetacek, 1994). Other species are omnivorous and still others are carnivorous, feeding on motile prey, such as dinoflagellates, flagellates and other copepods, (Lampitt, 1978; Kiørboe and Visser, 1999; Svensen and Kiørboe, 2000; Paffenho¨fer and Mazzocchi, 2002). Oithona is one of the major sources of food for many ichthyoplankton (Sa´nchez-Velasco, 1998), particularly for the larvae of commercially important species like cod, mackerel, seabream and hake (Young and Davis, 1992; Nip et al., 2003; Reiss et al., 2005). For some species, the availability of Oithona is crucial, as some fish larvae, at specific developmental stages, depend almost completely on this small copepod. This high specialization in feeding strategy, focusing on such small prey during a particular larval stage is shown by the specific mouth size and morphology of different predators and seems to be associated with avoidance of interspecific competition (Sassa and Kawaguchi, 2005). Strict dependence on specific food sources during critical developmental stages can have dramatic implications for the dynamics of several fish populations, as food limitation can affect recruitment severely (Olson and Olson, 1989). Carnivorous zooplankton such as chaetognaths (Saito and Kiørboe, 2001; Giesecke and Gonza´lez, 2004) and jellyfish (Omori et al., 1995; Buskey, 2003) also consume Oithona extensively, making these small copepods an important element in the structure of many food webs (Hansen et al., 2004). The significance of Oithona spp. in food webs is also implied by their continuously high abundances throughout the year and predominance during summer (Uye and Liang, 1998; Calbet et al., 2001; Keister and Peterson, 2003; Hansen et al., 2004), especially in the upper levels of the water column (Giesecke and Gonza´lez, 2004). Although Oithona has been described as one of the most abundant and possibly most important copepods in the world

(Gallienne and Robin, 2001), most studies on zooplankton communities have concentrated on larger taxa (Paffenho¨fer, 1993). The bias towards larger mesozooplankton can be attributed to the fact that most investigations have used medium sized plankton nets (Keister and Peterson, 2003; Albaina and Irigoien, 2004), which leads to the underestimation of smaller organisms (Gallienne and Robin, 2001). In addition to the lack of good estimates of small copepod abundances, there is also a general lack of studies of zooplankton variability in nearshore coastal waters at very shallow depths (Chisholm and Roff, 1990; Archambault et al., 1998; Seuront and Lagadeuc, 2001; Shanks et al., 2003). This is especially true for South Africa, where there have been only a few studies about the zooplankton of coastal waters (Barange and Boyd, 1992; Verheye et al., 1992; Huggett and Richardson, 2000; Thibault-Botha et al., 2004) and none about Oithona in the region. Insight into Oithona distribution in shallow inshore waters is also potentially important to our understanding of benthicepelagic dynamics, and recent studies on benthic ecological processes have focused on the role of benthic filter feeders as significant consumers of pelagic mesozooplankton (Davenport et al., 2000). The warm Agulhas current is the major offshore current on the south and east coasts of South Africa (Hunter, 1981; Goschen and Schumann, 1990; Goschen and Schumann, 1994). It flows towards the south-west, parallel to the coast at a maximum speed of 2.5 m s1, roughly following the 200 m isobath and diverging from the coast towards the south-east. Near the study area, it lies approximately 30 km offshore, but it can show dramatic onshore/offshore meanders, on occasions coming virtually into the intertidal region (Goschen and Schumann, 1990; Goschen and Schumann, 1994). The high degree of variability in the location of the front is likely to influence the distribution of zooplankton communities dramatically. While the plankton community may show long-term and regional stability, it is short-term and local variability that has the most direct effects on both consumers and prey populations. Thus, long-term and regional stability, shown by sampling at coarse temporal resolution and broad spatial scales, may mask variation at the time and spatial scales over which biological interactions occur. The present study is one of very few quantitative investigations (Hirota, 1990; Uye and Liang, 1998) of the spatiotemporal variability in zooplankton abundances in nearshore waters. It uses a relatively high time resolution sampling approach, at relatively local spatial scales and focuses on one of the most abundant components of the smallest copepod fraction, Oithona spp., especially Oithona plumifera. 2. Material and methods 2.1. Study sites The study was conducted between March 2000 and April 2001 at two sites 3 km apart, near Kenton-onSea (33 410 S, 26 400 E), on the south coast of South Africa (Fig. 1).

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Zooplankton availability in the nearshore water column was investigated as close to the shore as possible at Kenton (KE) and High Rocks (HR). At each site, three locations were identified, about 300 m apart (KEA, KEB, KEC and HRD, HRE, HRF; Fig. 1). This coast consists of dissipative shores with a permanent surf zone. Locations were just offshore of the surf zone. The distance from the shore changed with tide level and sea conditions, but was always within 500 m of the shore, and usually within 200e300 m (Fig. 1). The study area has equal semi-diurnal tides with a maximum range of 2e2.5 m. Current speed within the surf zone (0e10 m depths) varies between 0.04 and 0.21 m s1 (Phillips, personal communication). 2.2. Copepod abundance Sampling was done by means of vertical hauls using a plankton net with a mesh of 80 mm and a mouth of 30  30 cm: the net was pulled from approximately 1 m above the seabed (to minimise sand collection) to the surface, at a rate of about 0.5 m s1. The net did not show any evidence of clogging by larger phytoplankton. The depth of the water column ranged between 8 and 11 m. The volume of water filtered was calculated from the area of the mouth of the net and the depth of the haul. The position of each location was determined using a GPS (Global Positioning System) and, at each location, three replicate plankton samples were taken (Fig. 1).

The samples were preserved in a solution of 40% formalin and 60% sea water and returned to the laboratory for analysis. The contents of each sample were examined under a dissecting microscope and all copepods were separated and counted. Those samples with very high numbers of copepods were sub-sampled to one eighth or one sixteenth of the total sample using a Folsom plankton splitter. A sub-set of samples was also considered to identify Oithona at species level. Harpacticoid copepods were excluded from this study because sampling was done in very shallow waters where benthic organisms, such as most of the harpacticoids (INIDEP, 1981), could easily have been resuspended from the benthos by wave action and sampled in the water column. Oithona spp. adults were also separated from the rest of copepods and Oithona stages and used as a model to investigate spatio-temporal variability in small copepods. The abundance of the rest of the copepods in this study corresponded to the abundance of all copepods except Oithona spp. adults, harpacticoids and nauplii. We refer to these values as abundances of ‘‘other copepods’’. The abundances of Oithona spp. adults, nauplii and the other copepods were standardised to cubic meter. 2.3. Periodicity Temporal variation in other copepods, Oithona adults, and nauplii numbers was examined by sampling approximately fortnightly, as close as possible to spring tide, from March

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2000 to April 2001 (14 months), with a total of 21 plankton collections. The reduced number of sampling events (21 collections instead of 28) was due to bad sea conditions, when plankton sampling was not possible. 2.4. Statistical analysis All statistical analyses were performed using the software package Statistica 6. The study was initially planned as a spatially nested ANOVA design with location nested within site. However, Cochran’s test showed heteroscedasticity of data, even after log or square root transformation. Therefore, all data were analysed using the non-parametric KruskaleWallis and ManneWhitney tests. Separate analyses were run for Oithona adults, nauplii and other copepods. To examine temporal variation, the independent variable date was compared against abundance. The effects of the spatial components on abundance were examined by running 21 separate analyses for site and location using Bonferroni adjustment (Zar, 1996). 3. Results 3.1. Oithona adults’ variability In general, there was very high variability in abundance of adults belonging to the genus Oithona, with maximum mean values of over 6000 individuals per m3 on the 16 of April 2000 at KEC, and a minimum of zero at HRF on the 17 of October (Fig. 2). Abundances often varied dramatically between consecutive collections. For example, abundances of Oithona adults at KEC dropped from 6300 individuals per m3 to 100 and rose again to 1100 during the three consecutive collections of 16 April, 8 May and 16 May 2000 (Fig. 2). The processing of a sub-set of samples revealed that the Oithona community was consistently dominated by Oithona plumifera, which accounted between 73 and 94% for all identified Oithona. Oithona nana and an unidentified Oithona species (possibly Oithona simplex) contributed to less than 5% of total counts in all samples. There was no obvious seasonal trend in Oithona spp. abundance and the KruskaleWallis analysis showed no significant effect of date. Spatial variability of Oithona abundance was investigated at two levels: site (km scale) and location (100 m scale). In general, the distribution of Oithona amongst locations and sites was highly variable, with no clear trend at the location scale (Figs. 2 and 3). However, there were clear differences in abundances between sites, with more individuals generally occurring at KE than at HR (Fig. 3). ManneWhitney tests of the effect of site on each occasion, showed a significant effect in eight out of 21 tests, after Bonferroni adjustment (Table 1), with higher abundance of Oithona at KE than at HR on each of these occasions (Fig. 3). To investigate the effect of location on the variability of Oithona abundance, KruskaleWallis tests were done for

each of the 21 collections, again, using Bonferroni adjustment. Before Bonferroni adjustment, location seemed to have a significant effect on 13 out of 21 occasions. However, Bonferroni adjustment had a dramatic effect on the results, with the location effect disappearing from all comparisons (Table 1). Therefore, despite enormous variability among samples separated by 100 m, location had no significant effect on Oithona abundance. 3.2. Other copepods and nauplii variability Spatial variability at site and location scales was also assessed for other copepods and for nauplii. The spatial variability for these organisms showed similar spatial patterns to Oithona, with no clear location effect and, when the effect of site was significant, more individuals were found at KE than at HR (Figs. 4 and 5). ManneWhitney tests found site to have a significant effect on abundances on six out of 21 and three out of 21 occasions for other copepods and nauplii, respectively, after Bonferroni adjustment (Table 2). In general, fortnightly temporal scale at which sampling was done in this study, never had a significant effect on the abundance of other copepods, Oithona or nauplii (Figs. 2e 5). Of the two spatial variables explored, only the larger scale (site, km scale) had a significant effect on the distribution of other copepods, Oithona and nauplii, while the smaller scale (location at 100 m scale) did not affect abundance of any group. This indicates that patterns of abundances in the water column of the taxa examined differed randomly with time throughout the 14-month study. Abundances of the three groupings analysed were generally higher at KE than at HR, although because of high within-site variability, the differences were significant on relatively few occasions. 4. Discussion Although many studies of zooplankton communities focus on the importance of copepods in their role as a source of food for other organisms, a few examine the potential impact of smaller species on the lower levels of the food chains (Gonza´lez and Smetacek, 1994; Soussi et al., 2000). Organisms that are less than 500 mm in size easily outnumber larger copepods, especially in the upper levels of the water column (Falk-Petersen et al., 1999). Copepods play a crucial role in food-web dynamics, but small copepods are particularly important in the food webs of tropical and sub-tropical waters (Calbet et al., 2000). Their small size also implies that, as they feed on smaller particles, they will have a strong effect on the smaller food fractions and on phytoplankton availability (Kiørboe and Nielsen, 1994). However, the availability and abundance of small copepods in the water column have usually been underestimated due to the large mesh sizes commonly used in mesozooplankton studies (Gallienne and Robin, 2001; Hopcroft et al., 2005). The most common size of mesh for plankton sampling ranges between 200 and

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330 mm (Pinca and Dallot, 1997), which does not provide accurate estimates of the smaller fraction of the zooplankton. To our knowledge, the present study is the first quantitative description of the abundance of small adult copepods from the genus Oithona (particularly Oithona plumifera) at different

spatial scales in nearshore open coast waters. In interpreting our results, we recognise that sampling on different time scales, particularly finer time scales, may have produced different patterns. Nevertheless, the results showed no clear long-term trend or seasonality in the abundance of Oithona. On the contrary,

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dramatic changes in the numbers of organisms between subsequent collections were frequent (e.g. Fig. 3). Spatially, abundances varied enormously on scales of hundreds of meters, but with no consistent effect of location (i.e. there was random variation among locations), while at kilometer scales, more organisms were found at Kenton than at High Rocks. Table 1 Spatial variability in Oithona spp. adult abundance. Site (KruskaleWallis) and location (ManneWhitney) effects. Significant p-values in bold (critical p ¼ 0.0024 after Bonferroni adjustment)

20 March 2000 30 March 2000 8 April 2000 16 April 2000 8 May 2000 16 May 2000 3 June 2000 14 June 2000 30 July 2000 15 August 2000 29 September 2000 17 October 2000 4 November 2000 12 November 2000 29 November 2000 22 December 2000 21 January 2001 6 February 2001 26 March 2001 7 April 2001 24 April 2001

Site (n ¼ 2)

Location (n ¼ 6)

n.s. n.s. n.s. n.s. n.s. 0.0003 0.0023 n.s. n.s. n.s. n.s. 0.0017 0.001 0.002 n.s. n.s. 0.0003 n.s. 0.0003 n.s. 0.0004

n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s.

In contrast, a study in the North Sea (Nielsen and Sabatini, 1996) showed little temporal or spatial variability of Oithona biomass, suggesting that Oithona could be a constant food source for ichthyoplankton and planktivorous fishes. However, this study was carried out over only 12 days and involved extrapolation from the literature. More convincingly, Mazzocchi and Ribera d’Alcala’ (1995) sampled at fine temporal scales (every two weeks) from 1984 to 1990 and found that copepod populations in the Gulf of Naples were relatively constant throughout their seven year study. They suggested that only strong environmental changes or sudden catastrophes would seriously alter coastal zooplankton community structure. These results do not match with our findings and this could simply be due to biogeography or to differences in large-scale hydrodynamics. The sampling by Mazzocchi and Ribera d’Alcala’ (1995) was done about 3 km offshore at a permanent station 70 m deep and the North Sea study was conducted much farther offshore, while the present study was done very close inshore (<0.5 km). The shallow bottom topography of nearshore waters and the vicinity to the coastline affect water movement and transport of zooplankton dramatically and can be major determinants for temporal and spatial variabilities in the zooplankton (Pineda, 2000). As our sampling was conducted regularly at spring tide and at very shallow depths, the effect of turbulence, enhanced by tidal mixing (Howarth et al., 2002), could also be important in preventing zooplankton retention and aggregational swarming behaviour (Petersen et al., 1998; Ambler, 2002). In this study, differential distribution of Oithona at kilometer scales can likely be explained by both physical and

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biological factors. Biologically, predation, active movement, vertical migration or reproduction can influence the dynamics and abundance of zooplankton communities, resulting in different spatial aggregations (Folt and Burns, 1999). Diurnal swarming behaviour could also account for spatial distribution of oithonids (Buskey et al., 1996; Ambler, 2002). However,

temporal variability in our findings was so great that entirely biological explanations seem inadequate. For example, abrupt decreases in abundance can be attributed to mortality, including predation, but increases by orders of magnitude between events are best explained by physical aggregation. Also, biological processes tend to account for spatial structuring at

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718

Table 2 Spatial variability in other copepods (i.e. Oithonidae, harpacticoids, nauplii omitted) and naupliar abundances. Site (KruskaleWallis) and location (ManneWhitney) effects. Critical p-value in bold ( p ¼ 0.0024 after Bonferroni adjustment) Nauplii

20 March 2000 30 March 2000 8 April 2000 16 April 2000 8 May 2000 16 May 2000 3 June 2000 14 June 2000 30 July 2000 15 August 2000 29 September 2000 17 October 2000 4 November 2000 12 November 2000 29 November 2000 22 December2000 21 January 2001 6 February 2001 26 March 2001 7 April 2001 24 April 2001

Other copepods

Site (n ¼ 2)

Location (n ¼ 6)

Site (n ¼ 2)

Location (n ¼ 6)

n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. 0.0012 0.00004 n.s. n.s. n.s. 0.00016 n.s. n.s. n.s. n.s.

n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s.

n.s. n.s. n.s. n.s. n.s. 0.0018 0.00016 n.s. n.s. n.s. n.s. 0.00016 0.00004 n.s. n.s. n.s. 0.00004 n.s. n.s. n.s. 0.0005

n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. n.s. 0.0015

small scales (up to 100 m), while physical interactions seem to explain spatial variability and patchiness at scales larger than 100 m (Folt and Burns, 1999). Thus, we believe that these results illustrate the effects of hydrodynamics, particularly local advection, in shaping the spatial distribution of the copepod community. It is not uncommon for hydrodynamics to determine zooplankton distribution at kilometer scales (Wing et al., 1998, for 5.5e 9 km scales; Natunewicz and Epifanio, 2001 around 2.4 km; Ross, 2001) and local hydrodynamic processes could aggregate zooplankton at one site rather than another (in this case at Kenton rather than High Rocks). This, in turn, has implications for the benthic communities, as there is growing evidence that nearshore plankton dynamics drive process rates in intertidal systems (Menge et al., 1997; Connolly and Roughgarden, 1998; Pineda, 2000). Our results also have implications for the links between the benthic and inshore pelagic environments. Although we recognise that nauplii abundance might have been quantitatively underestimated due to the relatively large mesh used in the study, the relative patterns of spatial distribution observed for the other copepods and for nauplii confirm the trends identified for Oithona, with no clear patterns at 100 m scales, but with generally more individuals at Kenton than High Rocks. This supports physical over biological explanations and again suggests that local hydrodynamic conditions, driven by bottom topography and water velocity, favour the accumulation of generally small zooplankton at one site rather than the other. Patterns of local inshore hydrodynamics are extremely variable and change over long and

short temporal scales, making the distribution of zooplankton very patchy (Pulfrich, 1997; Stoner and Davis, 1997) and, in this particular case, making the densities of Oithona, especially Oithona plumifera, other copepods and, possibly, nauplii highly unpredictable. Finally, the irregular patchiness and extreme variability in abundance of Oithona found in the present study make this group of small copepods an unpredictable source of food for benthic consumers, and also for predators like ichthyoplankton and carnivorous zooplankton. Benthic filter feeders such as mussels can shift diet preference depending on the availability of food sources in the nearshore waters (Alfaro, 2006). As recent studies have shown, mussels are able to digest and extract energy from small crustaceans, allowing a certain degree of carnivory (Davenport et al., 2000). Therefore, it is possible that physical aggregation of small zooplankton at particular sites implies greater food availability for benthic filter feeders at those sites. 5. Conclusions In general, the results of this study suggest that the abundance of the smallest fraction of zooplankton is extremely variable and unpredictable in nearshore waters. However, the identification of similar patterns in separate analyses of three copepod groups strongly indicates that patchiness is driven by nearshore hydrodynamics operating at kilometer scales that favour some sites over others. Future studies on inshore zooplankton variability should use information on the characteristics of small scale water currents driven by the interaction of nearshore topography and wind-driven currents (e.g. Shanks et al., 2003). Acknowledgements This contribution was supported by funds from Rhodes University and the Andrew W. Mellon scholarship of Rhodes University as part of F.P. doctorate. We would like to thank V. Meaton for sorting the plankton samples and identification of Oithona spp. We also thank all who assisted in the field, during plankton collection. References Albaina, A., Irigoien, X., 2004. Relationships between frontal structures and zooplankton communities along a cross-shelf transect in the Bay of Biscay (1995 to 2003). Marine Ecology Progress Series 284, 65e75. Alfaro, A.C., 2006. Evidence of cannibalism and bentho-pelagic coupling within the life cycle of the mussel, Perna canaliculus. Journal of Experimental Marine Biology and Ecology 329, 206e217. Ambler, J.W., 2002. Zooplankton swarms: characteristics, proximal cues and proposed advantages. Hydrobiologia 480, 155e164. Archambault, P., Roff, J.C., Bourget, E., Bang, B., Ingram, G.I., 1998. Nearshore abundance of zooplankton in relation to shoreline configuration and mechanisms involved. Journal of Plankton Research 20, 671e690. Barange, M., Boyd, A.J., 1992. Life history, circulation and maintenance of Nyctiphanes capensis (Euphausiacea) in the northern Benguela system. South African Journal of Marine Science 12, 95e106.

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