IntroductionTop

Shelf-slope fronts separating low-salinity coastal waters from high-salinity open-sea waters are common along continental shelves (Wang et al. 1988Wang D., Vieira M.E.C., Salat J., et al. 1988. A shelf/slope frontal filament off the northeast Spanish Coast. J. Mar. Res. 46: 321-332., Houghton 1997Houghton R.W. 1997. Lagrangian flow at the foot of a shelfbreak front using a dye tracer injected into the bottom boundary layer. Geophys. Res. Lett. 24: 2035.). Physical and biological coupling in these frontal zones shows strong spatio-temporal variability as a result of hydrographic complexity and the activity of the organisms (Mackas et al. 1985Mackas D.L., Denman K.L., Abbott M.R. 1985. Plankton patchiness: biology in the physical vernacular. Bull. Mar. Sci. 37: 652-674., Sournia 1994Sournia A. 1994. Pelagic biogeography and fronts. Prog. Oceanogr. 34: 109-120.). In general, shelf-slope fronts are highly productive due to the accumulation and active growth of microalgae and zooplankters (Sabatés et al. 1989Sabatés A., Gili J.M., Pagès F. 1989. Relationship between zooplankton distribution, geographic characteristics and hydrographic patterns of the Catalan coast. Mar. Biol. 103: 153-159., Fernández et al. 1993Fernández E., Cabal J., Acuña J.L., et al. 1993. Plankton distribution across a slope current-induced front in the southern Bay of Biscay. J. Plankton Res. 15: 619-641., Mann and Lazier 2006Mann K.H., Lazier J.R.N. 2006. Dynamics of marine ecosystems: Biological-physical interactions in the oceans. Blackwell Publishing, Boston, 496 pp.). These phenomena determine the distributions and abundance of many groups of zooplankton (e.g. Kahru et al. 1984Kahru M., Elkenl J., Kotta I., et al. 1984. Plankton distributions and processes across a front in the open Baltic Sea. Mar. Ecol. Prog. Ser. 20: 101-111., Nishikawa et al. 1995Nishikawa J., Tsuda A., Ishigaki T., et al. 1995. Distribution of euphausiids in the Kuroshio front and warm water tongue with special reference to the surface aggregation of Euphausia pacifica. J. Plankton Res. 17: 611-629., Sabatés and Olivar 1996Sabatés A., Olivar M.P. 1996. Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar. Ecol. Prog. Ser. 135: 11–20.).

Gelatinous zooplankton are abundant in pelagic communities, playing an important role in food-web dynamics due to their great trophic impacts and rapid population growth, which sometimes results in seasonal blooms (Graham et al. 2001Graham W.M., Pagès F., Hamner W.M. 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451: 199-212., Pagès et al. 2001Pagès F., González H.E., Ramón M., et al. 2001. Gelatinous zooplankton assemblages associated with water masses in the Humboldt Current System, and potential predatory impact by Bassia bassensis (Siphonophora: Calycophorae). Mar. Ecol. Prog. Ser. 210: 13-24.). Appropriately classified as plankton, gelatinous organisms have limited horizontal mobility, so their abundance and distribution patterns depend on hydrodynamic features such as gyres, clines and fronts. However, explicit evidence for this bio-physical coupling is scarce (e.g. Pagès and Gili 1992Pagès F., Gili J.M. 1992. Influence of Agulhas waters on the population structure of planktonic Cnidarians in the southern Benguela Region. Sci. Mar. 56: 109-123., Graham et al. 2001Graham W.M., Pagès F., Hamner W.M. 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451: 199-212., Pavez et al. 2010Pavez M.A., Landaeta M.F., Castro L.R., et al. 2010. Distribution of carnivorous gelatinous zooplankton in the upwelling zone off central Chile (austral spring 2001). J. Plankton Res. 32: 1051-1065.).

Off the Catalan coast (NW Mediterranean), the shelf-slope density front is a permanent structure defined by strong salinity gradients, separating low-salinity shelf waters from the more saline waters offshore (Font et al. 1988Font J., Salat J., Tintoré J. 1988. Permanent features of the circulation in the Catalan Sea. Oceanol. Acta 9: 51-57., Alvarez et al. 1996Alvarez A., Tintoré J., Sabatés A. 1996. Flow modification and shelf-slope exchange induced by a submarine canyon off the northeast Spanish coast. J. Geophys. Res. 101: 12043-12055.). It is present in the upper 300 to 400 m of the water column and usually intersects the surface over the 1000 m isobath. Associated with the front is the Northern Current flowing southwestward following the continental slope at 20 to 30 cm s^-l (Font et al. 1995Font J., Garcia-Ladona E., Gorriz E.G. 1995. The seasonality of mesoscale motion in the Northern Current of the western Mediterranean: several years of evidence. Oceanol. Acta 18: 207-219.). In spring, northern Catalan coastal waters experience strong spatial and temporal variability due to the large inputs of continental runoff, mainly from the Rhône River in the northern Gulf of Lions (Masó and Tintoré 1991Masó M., Tintoré J. 1991. Variability of the shelf water off the northeast Spanish coast. J. Mar. Syst. 1: 441-450., Sabatés et al. 2007Sabatés A., Salat J., Palomera I., et al. 2007. Advection of anchovy (Engraulis encrasicolus) larvae along the Catalan continental slope (NW Mediterranean). Fish. Oceanogr. 16: 130-141.). These relatively low-salinity waters, advected by the Northern Current along the shelf break, increase the mesoscale activity at the shelf-slope front, generating oscillations and eddies (Alvarez et al. 1996Alvarez A., Tintoré J., Sabatés A. 1996. Flow modification and shelf-slope exchange induced by a submarine canyon off the northeast Spanish coast. J. Geophys. Res. 101: 12043-12055., Flexas et al. 2002Flexas M., Durrieu de Madron X., Garcia M., et al. 2002. Flow variability in the Gulf of Lions during the MATER HFF experiment (March-May 1997). J. Mar. Syst. 33: 197-214.). The continental shelf in the study area (Fig. 1) is relatively narrow, with a submarine canyon whose head is close to the coast.

Previous studies in the area have analysed the role of the front and the associated current in primary and secondary production (Estrada 1991Estrada M. 1991. Phytoplankton assemblages across a NW Mediterranean front: changes from winter mixing to spring stratification. In: Ros J.D., Prat N. (eds), Homage to Ramon Margalef; or Why There Is Such Pleasure in Studying Nature, Oecol. Aquat. 10: 157-185., Estrada et al. 1999Estrada M., Varela R.A., Salat J., et al. 1999. Spatio-temporal variability of the winter phytoplankton distribution across the Catalan and North Balearic fronts (NW Mediterranean). J. Plankton Res. 21: 1-20., Alcaraz et al. 2007Alcaraz M., Calbet A., Estrada M., et al. 2007. Physical control of zooplankton communities in the Catalan Sea. Prog. Oceanogr. 74: 294-312.), and in zooplankton and ichthyoplankton distribution (Sabatés et al. 1989Sabatés A., Gili J.M., Pagès F. 1989. Relationship between zooplankton distribution, geographic characteristics and hydrographic patterns of the Catalan coast. Mar. Biol. 103: 153-159., Sabatés and Olivar 1996Sabatés A., Olivar M.P. 1996. Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar. Ecol. Prog. Ser. 135: 11–20., Sabatés et al. 2004Sabatés A., Salat J., Masó M. 2004. Spatial heterogeneity of fish larvae across a meandering current in the northwestern Mediterranean. Deep-Sea Res Pt I. 51: 545-557.). Recently, the importance of the front in the distributions of medusan species forming blooms, such as Pelagia noctiluca (Forsskål, 1775), has been reported (Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.). However, little is known about the influence of the shelf-slope front on the most abundant planktonic cnidarians, especially at short timescales.

The planktonic cnidarian community along the Catalan coast in spring is dominated by a few species. Siphonophorae constitute the bulk of the community, and the calycophoran Muggiaea atlantica Cunningham, 1892 is by far the most abundant and representative species. Among Hydromedusae, Aglaura hemistoma Péron and Lesueur, 1810, is the most abundant and widespread. Both species are neritic and epipelagic, accounting in the area for up to 95% of the planktonic cnidarian community in spring (Gili et al. 1987aGili J.M., Pagès F., Riera T. 1987a. Distribución de las especies más frecuentes de sifonóforos calicóforos en la zona norte del Mediterráneo occidental. Inv. Pesq. 51: 323-338., bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401.). Although these two species are present in the Mediterranean all year around (Bouillon et al. 2004Bouillon J., Medel M.D., Pagès F., et al. 2004. Fauna of the Mediterranean Hydrozoa. Sci. Mar. 68(Suppl. 2): 5-438.), the highest abundances of M. atlantica in the northwestern basin have been recorded from April to June (Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro et al. 2012Licandro P., Souissi S., Ibañez F., et al. 2012. Long-term variability and environmental preferences of calycophoran siphonophores in the Bay of Villefranche (north-western Mediterranean). Prog. Oceanogr. 97-100: 152–163.), and peaks of Aglaura hemistoma occur between June and September (Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro and Ibañez 2000Licandro P., Ibañez F. 2000. Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors. J. Plankton Res. 22: 2225-2253.). Both species are particularly abundant in the first 50 m of the water column but can occur down to 200 m (Gili et al. 1987aGili J.M., Pagès F., Riera T. 1987a. Distribución de las especies más frecuentes de sifonóforos calicóforos en la zona norte del Mediterráneo occidental. Inv. Pesq. 51: 323-338., bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., Batistić et al. 2004Batistić M., Kršinić F., Jasprica N., et al. 2004. Gelatinous invertebrate zooplankton of the South Adriatic: species composition and vertical distribution. J. Plankton Res. 26: 459-474.). The value of knowing the abundance and distribution patterns of planktonic cnidarians derives from their predation on most other zooplankton (e.g. Biggs 1977Biggs D.C. 1977. Field studies of fishing, feeding, and digestion in siphonophores. Mar. Behav. Physiol. 4: 261-274., Purcell 1997Purcell J.E. 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates, and effects on prey populations. Ann. Inst. Oceanogr. Paris. 73: 125-137., Colin et al. 2005Colin S.P., Costello J.H., Graham W.M., et al. 2005. Omnivory by the small cosmopolitan hydromedusa Aglaura hemistoma. Limnol. Oceanogr. 50: 1264-1268.), affecting the structure and dynamics of the whole planktonic community.

Our goal was to investigate how the variability of hydrodynamic structures determines the mesoscale distributions of planktonic cnidarians. Our approach was to study the coupling between short-term variability in the location of the shelf-slope front and the distributions of M. atlantica and A. hemistoma. To achieve this aim, we analysed the changes in abundance and spatial distribution of both species during three cross-frontal surveys carried out at approximately 10-day intervals.

MaterialS and methods

The study area is located off the northern Catalan coast, NW Mediterranean (Fig. 1). Three oceanographic cruises were carried out from mid-May to late June 1992, at approximately 10-day intervals (13-21 May, 2-9 June and 18-25 June). On each survey, 43-44 stations were sampled for environmental and biological parameters. Stations were located approximately 8.5 km apart, and distributed along seven transects perpendicular to the shoreline, from near the coast to beyond the shelf-slope front. An additional transect in the northernmost part of the area (grey dots in Fig. 1) was conducted for environmental measurements only. Vertical profiles of basic hydrographic variables (temperature, salinity and fluorescence) were obtained at each station using a Mark-III Neil Brown CTD probe equipped with a Sea Tech fluorometer. Maps of the horizontal distribution of each environmental parameter (at 10 m depth) were generated by gvSIG (OADE-2010) and ArcGIS 10.2 software, applying the spline interpolations with a cell size of 200 m (see Fig. 2). The Catalano-Balearic Sea bathymetric chart (2005) was used to represent the bathymetry at 100 m intervals.

Zooplankton samples were collected using a bongo net of 60 cm mouth diameter and 300 µm mesh. Oblique hauls were performed, integrating the water column from a maximum depth of 200 m (or 5 m above the bottom in stations shallower than 200 m) to the surface. Samples were preserved immediately after collection in a 5% solution of formaldehyde in seawater buffered with borax. The volume of filtered water was estimated by means of a flowmeter placed in the centre of the net mouth.

In the laboratory, after the cruises took place, the siphonophore M. atlantica (polygastric stage) and the hydromedusa A. hemistoma were identified and counted under a stereomicroscope. Counts were standardized to number of individuals per 1000 m³. Recently, to complete the study with the rest of the cnidarian community, analysis of those same samples were carried out, however we found that the morphological conditions of the individuals had impoverished so much that the taxonomical identifications were not possible. The exceptional oceanographic conditions in which the cruises were performed and the ecological importance of these two species encouraged us to proceed with the study presented here.

Statistical analysis

The potential explanatory relationships between species abundance and the environmental variables: surface (10 m depth) salinity, fluorescence and temperature, and bottom depth were tested separately in each surveyed situation by fitting generalized additive models (GAMs), which account for non-linear changes in abundance with the environmental variables by applying other than Gaussian data distributions. The models were fitted with an error distribution from the negative binomial family and a log link function (Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp.), using the “mgcv” package (Wood 2014Wood S.N. 2014. mgcv: Mixed GAM Computation Vehicle with GCV/AIC/REML smoothness estimation. R package version 1.8-3.). To eliminate bias due to varying sampling units (volumes of seawater filtered by the net), we included the log of filtered volume as an offset inside the model (Penston et al. 2008Penston M.J., Millar C.P., Zuur A.F., et al. 2008. Spatial and temporal distribution of Lepeophtheirus salmonis (Krøyer) larvae in a sea loch containing Atlantic salmon, Salmo salar L., farms on the north-west coast of Scotland. J. Fish Dis. 31: 361-371., Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp., Guerrero et al. 2013Guerrero E., Gili J.M., Rodriguez C.S., et al. 2013. Biodiversity and distribution patterns of planktonic cnidarians in San Matías Gulf, Patagonia, Argentina. Mar. Ecol. 34: 71–82.). Spatial autocorrelation of samples was checked by plotting the residual of the models in a variogram (Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp.); in all cases no spatial correlation was suggested and spatial independence was assumed.

GAM analyses were performed in two steps (Zarauz et al. 2007Zarauz L., Irigoien X., Urtizberea A., et al. 2007. Mapping plankton distribution in the Bay of Biscay during three consecutive spring surveys. Mar. Ecol. Prog. Ser. 345: 27-39., Silva et al. 2014Silva T., Gislason A., Licandro P., et al. 2014. Long-term changes of euphausiids in shelf and oceanic habitats southwest, south and southeast of Iceland. J. Plankton Res. 36: 1262-1278.). First, GAMs were based on single explanatory variables to study the influence of each hydrographic parameter on the species abundance. Later, GAMs of increasing complexity were applied, combining multiple explanatory variables. In the first, we allowed information on collinear variables; in the second, a more realistic situation was modelled in which all the parameters interact as in the environment. The amount of smoothing was minimized (k=3 to 5) to aid interpretation of the biological trends (Wood 2014Wood S.N. 2014. mgcv: Mixed GAM Computation Vehicle with GCV/AIC/REML smoothness estimation. R package version 1.8-3.). From among single variable-based GAMs, the best-fitting ones were selected based on the un-biased risk estimator (UBRE), the percentage of deviance explained, the smooth confidence region and the spread of the residual in the model validation step (Wood and Augustin 2002Wood S.N, Augustin N.H. 2002. GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecol. Model. 157: 157-177., Planque et al. 2007Planque B., Bellier E., Lazure P. 2007. Modelling potential spawning habitat of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) in the Bay of Biscay. Fish. Oceanogr. 16: 16-30., Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp., Silva et al. 2014Silva T., Gislason A., Licandro P., et al. 2014. Long-term changes of euphausiids in shelf and oceanic habitats southwest, south and southeast of Iceland. J. Plankton Res. 36: 1262-1278.). For multiple variable–based GAMs, collinearity between pairs of variables was evaluated by pairwise scatterplots, Pearson’s correlation coefficients (cut-off value |0.5|) and corroboration by the variance inflation factor (Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp.). In early June, salinity and fluorescence were collinear. Since salinity was the variable best representing the front (see Fig. 2), and was also the strongest predictor among the single variable GAMs for that cruise, it was kept. The variables for multivariable GAMs were chosen by a backward-elimination process for the least significant predictor based on the chi-square statistic. Best-fitting combined GAMs where selected based on the UBRE score (the lowest the best), the percentage of deviance explained (the highest the best) and the spread of the residuals in the model validation step (Zuur et al. 2009Zuur A.F., Ieno E.N., Walker N.J., et al. 2009. Mixed effects models and extension in ecology with R. Springer-Verlag, New York, 574 pp., Silva et al. 2014Silva T., Gislason A., Licandro P., et al. 2014. Long-term changes of euphausiids in shelf and oceanic habitats southwest, south and southeast of Iceland. J. Plankton Res. 36: 1262-1278.).

Differences in species abundance between the two sides of the front, when detected at the surface (in mid-May and early June), were tested for significance in order to know whether the front per se had an influence on the species abundance distribution. To this end, an analysis of variance was performed using generalized linear models (GLM) with the “glm.nb” package (Venables and Ripley 2002Venables W.N., Ripley B.D. 2002. Modern Applied Statistics with S. Springer, New York, 498 pp.), which fit a GLM with a negative binomial distribution. The model was applied with a log link function and an offset for the log of filtered volume in a way similar to that explained for GAMs. To identify the stations located on each side of the front, the geographical position of the front was defined from the maximum difference in salinity between adjacent stations on the same transect and between transects.

All analyses were performed using the free statistical software R, version 3.0.2 (R Development Core Team 2013R Development Core Team. 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. Available at: http://www.r-project.org/).

ResultsTop

Hydrographic conditions

In the first survey in mid-May, the salinity front was over the slope approximately 50 km offshore, running in a northeast to southwest direction. Maximum salinity values (~38.2) were recorded at the most offshore stations. A band of relatively low salinity (37.6-37.7) was observed between the shelf and the open sea, intensifying the salinity and density gradients over the slope. The highest fluorescence values (from 5 to 7 units) were mainly detected offshore in the northeastern area. The lowest temperatures (~14°C) were recorded in the northwestern corner of the grid, and the highest (17°C) were in the south (Fig. 2: A1-C1; Table 1).

In the second survey, ten days later in early June, a completely different spatial layout was found. The front, running parallel to the coast, was over the shelf at about 20 km from the coast, confining waters of low salinity (37.2) inshore and thus causing an intense salinity gradient. The highest fluorescence values (up to 13 units) were restricted to the inshore side of the front, associated with the low-salinity waters, while very low fluorescence values (<2) were measured on the offshore side. Temperature was higher than on the May cruise, showing a gradient from near the coast (17.5°C) towards the open sea (~19°C) (Fig. 2: A2-C2; Table 1).

In the third survey, in late June, no frontal structure was detected in the upper layers, and the salinity distribution was complex, with patches of low values covering the whole area (Fig. 2: A3). Fluorescence decreased offshore, and the highest values (from 3 to 7 units) appeared to be associated with areas of low salinity. During this survey, high temperatures were detected in coastal waters and offshore (~19.5°C) (Fig. 2: A3-C3, Table 1).

Spatio-temporal distribution of Muggiaea atlantica and Aglaura hemistoma

On all three cruises the mean abundance of M. atlantica was higher than that of A. hemistoma (Table 2). Abundance values for M. atlantica were high during the first two cruises (8640±11580 and 9378±18818 ind. 1000 m^–3, respectively) but lower during the last cruise (4008±3794 ind. 1000 m^–3). Aglaura hemistoma was relatively abundant on the first cruise (1759±343 ind. 1000 m^–3) but markedly lower on the two June cruises (128±286 and 478±845 ind. 1000 m^–3, respectively). For both species, the lowest frequency of occurrence was observed on the second cruise (86% and 52% for M. atlantica and A. hemistoma, respectively; Table 2).

High spatial variability in species abundance and distribution was observed over a short time scale (10 days), and in general both species displayed a similar onshore-offshore distribution pattern closely related to the variable location of the shelf-slope front (Fig. 3). In mid-May, M. atlantica and A. hemistoma were widely distributed over the whole study area, the location of the salinity front setting a clear limit for their distributions. Very low densities of M. atlantica were detected on the oceanic side of the front, and A. hemistoma was practically absent (Fig. 3: A1, B1). Higher densities of both species were observed at stations located over the edges of the submarine canyon than at those over the canyon axis (Fig. 3: A1, B1). Single variable-based GAMs revealed bottom depth as the strongest predictor for the spatial distribution of M. atlantica, explaining 47% of its variability, with a linear negative effect (Fig. 4: A1, Table 3). Depth was the second predictor for A. hemistoma (36%), with a negative effect from 500 m outwards (Fig. 5: A1, Table 3). Salinity was the second strongest predictor (41%) for M. atlantica and the first for A. hemistoma (57%, Table 3), and both species followed the same trend, positive up to ~37.9 (Fig. 4: B1) and ~37.8 (Fig. 5: B1), respectively, and decreasing above those values. Fluorescence was the third predictor for both species, whereas temperature was the least explanatory variable (Figs 4: C1-D1 and 5: C1-D1, Table 3).

In early June the spatial distribution of both species was restricted to a narrow belt over the shelf, limited offshore by the position of the front (Fig. 3: A2, B2). The abundance of M. atlantica was high close to the coast and very low on the open-ocean side of the front. Aglaura hemistoma showed the highest densities near to and inside the front, being almost absent on the offshore side of the front. Results of the single variable–based GAMs revealed salinity as the strongest explanatory variable for both the siphonophore (68%) and the hydromedusa (47%), with a marked decrease in abundance above ~37.3 for the former and a generally decreasing trend at higher salinity for the latter. As an exception, an increase was observed at ~37.6, corresponding to one of the isolines delimiting the salinity front (Figs 4: B2 and 5: B2; Table 3). Fluorescence was the second most important explanatory factor (56%) for M. atlantica, showing a positive effect up to ~7 with a plateau at higher values (Fig. 4: C2; Table 3). Temperature was the second most important variable for A. hemistoma (36%), with a negative trend in warmer waters (Fig. 5: D2; Table 3). The least significant variables during this period were bottom depth and temperature for M. atlantica (25.9% and 25.6%, respectively; Table 3) and bottom depth and fluorescence for A. hemistoma (33.0% and 32.8%, respectively; Table 3).

In late June, during the third cruise, as during the first cruise, the distributions of both species again covered a broad area, extending well beyond the shelf break, and higher densities of both species were recorded over the canyon flanks than at stations located over the canyon axis (Fig. 3: A3, B3). The GAMs showed bottom depth as the strongest explanatory variable for both species, explaining 37.4% for the siphonophore, with a negative effect from ~600 m outward (Fig. 4: A3, Table 3), and 31% for the hydromedusa with a linear negative effect (Fig. 5: A3, Table 3). Fluorescence was the second strongest predictor both for M. atlantica (36.9%), showing a positive effect up to ~3 (Fig. 4: C3, Table 3) and slightly negative above that, and for A. hemistoma (23%), showing a positive effect up to ~2.5 and slightly negative one at higher values (Fig. 5: A3, Table 3). Salinity was the third factor for both species, while temperature was not significant for the siphonophore and the least explanatory factor for the hydromedusa (Figs 4: B3, C3 and 5: B3, C3, Table 3).

The analyses conducted with the multiple variable-based GAMs revealed an improvement of up to twice the variability explained in comparison with those based on a single variable. Results showed that not all variables included in the analyses significantly contributed to the overall combined models, and the relative importance of the different explanatory variables varied in comparison with the single variable–based analysis, although displaying the same trends. The most significant variable was always coincident with the strongest one obtained with single GAMs (Tables 3 and 4). In mid-May, the best fitting combined model for M. atlantica explained 53% of deviance and included two significant variables: bottom depth and temperature. The best fitting combined model for A. hemistoma explained 71% of the distribution and included three significant variables: salinity, bottom depth and fluorescence. In early June, both species shared the same best model: salinity and (marginally significant) bottom depth explaining 70% and 50% for M. atlantica and A. hemistoma, respectively. In late June, bottom depth and fluorescence explained 68% of deviance of M. atlantica and for A. hemistoma the best model included all variables: bottom depth, salinity, fluorescence and temperature explaining 63% of deviance (Table 4).

The GLM results showed significantly higher abundances for both M. atlantica and A. hemistoma on the inshore side of the front than on the offshore side (M. atlantica: z-value =–10.67, p<0.001, A. hemistoma: z-value =–9.410, p-value<0.001) (Fig. 6).

DISCUSSIONTop

The temporal scale of the sampling allowed us to identify the short-term spatial variability of the shelf-slope density front and the responses of M. atlantica and A. hemistoma species to associated environmental changes. The shifting position of the front is characteristic of the spring period off the northern Catalan coast, and results from the advection of low-salinity waters by the Northern Current (Alvarez et al. 1996Alvarez A., Tintoré J., Sabatés A. 1996. Flow modification and shelf-slope exchange induced by a submarine canyon off the northeast Spanish coast. J. Geophys. Res. 101: 12043-12055., Masó et al. 1998Masó M., Sabatés A., Olivar M.P. 1998. Short-term physical and biological variability in the shelf-slope region of the NW Mediterranean during the spring transition period. Cont. Shelf Res. 18: 661-675., Sabatés et al. 2007Sabatés A., Salat J., Palomera I., et al. 2007. Advection of anchovy (Engraulis encrasicolus) larvae along the Catalan continental slope (NW Mediterranean). Fish. Oceanogr. 16: 130-141.). The low-salinity waters originating in the Gulf of Lions, mainly due to the River Rhône outflow, help strengthen the gradient of the shelf-slope density front. The temporal scale at which the frontal system oscillates has been reported to exert a decisive influence on processes affecting the concentration and dispersal of zooplankton and fish larvae (Sabatés and Olivar 1996Sabatés A., Olivar M.P. 1996. Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar. Ecol. Prog. Ser. 135: 11–20., Masó et al. 1998Masó M., Sabatés A., Olivar M.P. 1998. Short-term physical and biological variability in the shelf-slope region of the NW Mediterranean during the spring transition period. Cont. Shelf Res. 18: 661-675., Sabatés et al. 2004Sabatés A., Salat J., Masó M. 2004. Spatial heterogeneity of fish larvae across a meandering current in the northwestern Mediterranean. Deep-Sea Res Pt I. 51: 545-557.). The gelatinous zooplankton followed a similar trend, varying in their spatial distributions at short time scales. The two cnidarian species studied are epipelagic, mainly occurring in the surface layer between 0 and 50 m (Gili et al. 1987aGili J.M., Pagès F., Riera T. 1987a. Distribución de las especies más frecuentes de sifonóforos calicóforos en la zona norte del Mediterráneo occidental. Inv. Pesq. 51: 323-338., bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170.), and holoplanktonic, making them particularly susceptible to surface-water dynamics (Mackie et al. 1987Mackie G.O., Pugh P.R., Purcell J.E. 1987. Siphonophore Biology. Adv. Mar. Biol. 24: 97-262., Blackett et al. 2014Blackett M., Licandro P., Coombs S.H., et al. 2014. Long-term variability of the siphonophores Muggiaea atlantica and M. kochi in the Western English Channel. Prog. Oceanogr. 128: 1-14.).

The abundance values recorded for both species are in accordance with previous reports in the area during the same season (Gili 1986Gili J.M. 1986. Estudio sistemático y faunístico de los cnidarios de la Costa Catalana. Ph.D. thesis. Univ. Autónoma Barcelona, 634 pp., Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.). The higher mean abundance of M. atlantica, compared with A. hemistoma, is usual in the NW Mediterranean (Gili et al. 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro and Ibañez 2000Licandro P., Ibañez F. 2000. Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors. J. Plankton Res. 22: 2225-2253., Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.), and it has been observed since M. atlantica replaced the formerly dominant, congeneric species Muggiaea kochii (Will, 1844) (Kršinić and Njire 2001Kršinić F., Njire J. 2001. An invasion by Muggiaea atlantica Cunningham 1892 in the northern Adriatic Sea in the summer of 1997 and the fate of small copepods. Acta Adriatica 42: 49-59., Batistić et al. 2007Batistić M., Jasprica N., Caric M., et al. 2007. Annual cycle of the gelatinous invertebrate zooplankton of the eastern South Adriatic coast (NE Mediterranean). J. Plankton Res. 29: 671-686., Licandro et al. 2012Licandro P., Souissi S., Ibañez F., et al. 2012. Long-term variability and environmental preferences of calycophoran siphonophores in the Bay of Villefranche (north-western Mediterranean). Prog. Oceanogr. 97-100: 152–163.). However, the hydromedusa can display peaks of greater abundance at some periods of the year (Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., Licandro and Ibañez 2000Licandro P., Ibañez F. 2000. Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors. J. Plankton Res. 22: 2225-2253.). Both species varied considerably in their mean abundance between surveys. For M. atlantica the temporal abundance sequence agrees with the seasonal trend previously observed in the NW Mediterranean. The highest values are generally recorded from April to June, significantly decreasing at the end of June and in July (Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro and Ibañez 2000Licandro P., Ibañez F. 2000. Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors. J. Plankton Res. 22: 2225-2253.). The highest abundance of A. hemistoma was observed in May, and it decreased markedly in June. That pattern contrasts with previous observations of the highest seasonal densities for it in June and July, after much lower values in May (Gili et al. 1987bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro and Ibañez 2000Licandro P., Ibañez F. 2000. Changes of zooplankton communities in the Gulf of Tigullio (Ligurian Sea, Western Mediterranean) from 1985 to 1995. Influence of hydroclimatic factors. J. Plankton Res. 22: 2225-2253.). The inflow of low-salinity waters detected in early June inshore of the front could have negatively affected the abundance of A. hemistoma (Fig. 3: B2, Table 2). However, as this species has been observed inhabiting areas of similar and lower salinity (e.g.: Gili et al. 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Nagata et al. 2014Nagata R.M., Nogueira Júnior M., Brandini F.P., et al. 2014. Spatial and temporal variation of planktonic cnidarian density in subtropical waters of the Southern Brazilian Bight. J. Mar. Biol. Assoc. UK 94: 1387-1400.), factors other than salinity per se probably affected its abundance.

Muggiaea atlantica and A. hemistoma displayed high spatio-temporal variability in the brief study period, apparently driven by the rapid onshore-offshore displacements of the shelf-slope front. Both species occurred predominantly inshore of the front, with significantly higher abundances there than on the offshore side (Figs 3 and 4). Previous studies in the region have also reported the highest concentration of M. atlantica and A. hemistoma on the inshore side of the front (Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.). The front acts as a natural barrier, limiting the distribution seaward of both species; this phenomenon has also been documented for larvae of coastal fish in the study area, with the front preventing their displacement to the open sea (Sabatés and Olivar 1996Sabatés A., Olivar M.P. 1996. Variation of larval fish distributions associated with variability in the location of a shelf-slope front. Mar. Ecol. Prog. Ser. 135: 11–20., Sabatés et al. 2004Sabatés A., Salat J., Masó M. 2004. Spatial heterogeneity of fish larvae across a meandering current in the northwestern Mediterranean. Deep-Sea Res Pt I. 51: 545-557.). In the case of the jellyfish, in addition to the barrier effect of the density front, we must consider that since they are mainly water with the same ionic concentration as the surrounding seawater, they tend to remain in waters of similar salinity (Graham et al. 2001Graham W.M., Pagès F., Hamner W.M. 2001. A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451: 199-212.). The accumulation over the shelf, very strong for M. atlantica when the front was close to the coast, could lead to high predation pressure on their planktonic prey; this species is known to be an effective predator, particularly on copepods (Purcell 1982Purcell J.E. 1982. Feeding and growth of the siphonophore Muggiaea atlantica (Cunningham 1893). J. Exp. Mar. Bio. Ecol. 62: 39-54.), and when siphonophores are very abundant they can significantly affect planktonic populations (Purcell 1981Purcell J.E. 1981. Feeding ecology of Rhizophysa eysenhardti, a siphonophore predator of fish larvae. Limnol. Oceanogr. 26: 424-432., Purcell and Kremer 1983Purcell J.E, Kremer P. 1983. Feeding and metabolism of the siphonophore Sphaeronectes gracilis. J. Plankton Res. 5: 95-106.). Other dominant jellyfish species in the area, the siphonophores Lensia subtilis (Chun, 1886) and Chelophyes appendiculata (Eschscholtz, 1829) and the hydromedusae Rhopalonema velatum Gegenbaur, 1857 and Solmundella bitentaculata (Quoy and Gaimard, 1833), have also been reported to display similar patterns, with maximum abundances on the coastal side of the density front (Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.). However, oceanic species such as the siphonophore Lensia conoidea (Keferstein and Ehlers, 1860) and the scyphomedusa Pelagia notiluca were more abundant in the frontal area and offshore (Sabatés et al. 2010Sabatés A., Pagès F., Atienza D., et al. 2010. Planktonic cnidarian distribution and feeding of Pelagia noctiluca in the NW Mediterranean Sea. Hydrobiologia 645: 153-165.). Thus, the front seems to exert a barrier effect for both neritic and oceanic species, limiting their offshore and inshore displacement, respectively.

Studies conducted in other geographical areas have also shown the role of fronts shaping the distributions of gelatinous zooplankton. Analogies are found, for instance, in the salinity-driven mesoscale front in the Southern California Bight, where most gelatinous zooplankton organisms were located on the inshore side of the front (Luo et al. 2014Luo J.Y., Grassian B., Tang D., et al. 2014. Environmental drivers of the fine-scale distribution of a gelatinous zooplankton community across a mesoscale front. Mar. Ecol. Prog. Ser. 510: 129-149.). Pavez et al. (2010)Pavez M.A., Landaeta M.F., Castro L.R., et al. 2010. Distribution of carnivorous gelatinous zooplankton in the upwelling zone off central Chile (austral spring 2001). J. Plankton Res. 32: 1051-1065. also found the highest abundance of gelatinous zooplankton (hydromedusae, siphonophores and ctenophores) at the neritic inshore stations of a density front off central Chile. However, M. atlantica, evenly distributed over the shelf and slope, did not prove to be influenced by the position of the front. By contrast, the seasonal thermohaline front in the southern Benguela Region delimited the distribution of most species to the offshore side of the front (Pagès and Gili 1992Pagès F., Gili J.M. 1992. Influence of Agulhas waters on the population structure of planktonic Cnidarians in the southern Benguela Region. Sci. Mar. 56: 109-123.). High abundances of A. hemistoma and M. atlantica were detected over the edge of the continental shelf, offshore of the front, in relation to the intrusion of Agulhas water, whose input increases the gelatinous zooplankton density and diversity. In general, the different hydrodynamic variability associated with each frontal system is a key factor explaining the spatial heterogeneity of plankton distribution (Le Fèvre 1986Le Fèvre J. 1986. Aspects of the biology of frontal systems. Adv. Mar. Biol. 23: 163-299.).

The measured environmental parameters appeared to have important effects on the distributions and abundance of the two species. Bottom depth and salinity were the variables most closely related to the distribution patterns (Tables 3 and 4). When the front was located away from the coast, M. atlantica and A. hemistoma abundances gradually decreased with bottom depth. This trend has already been documented by other studies on the area (Gili et al. 1987aGili J.M., Pagès F., Riera T. 1987a. Distribución de las especies más frecuentes de sifonóforos calicóforos en la zona norte del Mediterráneo occidental. Inv. Pesq. 51: 323-338., bGili J.M., Pagès F., Vives F. 1987b. Distribution and ecology of a population of planktonic cnidarians in the western Mediterranean. In: Bouillon J., Boero F., Cicogna F., et al. (eds), Modern Trends in the Systematics, Ecology, and Evolution of Hydroids and Hydromedusae, Oxford University Press, Oxford, UK; pp. 157-170., 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401.) and is in agreement with the neritic character of both species. Abundances also declined at the higher salinity values (see Figs 3, 4 and 5) characterizing waters on the seaward side of the front. In particular, when the front occurred over the shelf in early June, salinity was the variable most strongly related to the spatial distributions of both species (Tables 3 and 4). Salinity has previously been reported as a determinant factor for the distributions and abundance of gelatinous zooplankton at various locations in the NW Mediterranean (Gili et al. 1988Gili J.M., Pagès F., Sabatés A., et al. 1988. Small-scale distribution of a cnidarian population in the western Mediterranean. J. Plankton Res. 10: 385-401., Licandro et al. 2012Licandro P., Souissi S., Ibañez F., et al. 2012. Long-term variability and environmental preferences of calycophoran siphonophores in the Bay of Villefranche (north-western Mediterranean). Prog. Oceanogr. 97-100: 152–163.) and the North Atlantic (Blackett et al. 2014Blackett M., Licandro P., Coombs S.H., et al. 2014. Long-term variability of the siphonophores Muggiaea atlantica and M. kochi in the Western English Channel. Prog. Oceanogr. 128: 1-14., Greer et al. 2015Greer A.T., Cowen R.K., Guigand C.M., et al. 2015. Fine-scale planktonic habitat partitioning at a shelf-slope front revealed by a high-resolution imaging system. J. Mar. Syst. 142: 111–125.).

High fluorescence values were clearly associated with the presence of low-salinity waters. These waters come from the Rhône River runoff, advected by the Northern Current along the Catalan coast, and are highly productive at surface; the offshore location of these low-salinity waters is variable due to the horizontal oscillation of the shelf-slope front (Sabatés et al. 2007Sabatés A., Salat J., Palomera I., et al. 2007. Advection of anchovy (Engraulis encrasicolus) larvae along the Catalan continental slope (NW Mediterranean). Fish. Oceanogr. 16: 130-141.). Abundance of both species in relation to fluorescence showed different trends (almost opposite) in mid-May to those of the two June cruises (Figs 4 and 5). In mid-May high fluorescence values were located offshore, coinciding with low abundance values for M. atlantica and A. hemistoma. In June high fluorescence values were detected on the inshore side of the front at stations where the two species were particularly abundant (Figs 2 and 3). This suggests that productive waters per se had no direct effect on the abundance of either species, depth being in fact the responsible variable.

No clear trend in the distribution of the species was detected regarding temperature. Although both species showed lower abundance in warmer waters, the narrow temperature variability within each survey and the short seasonal period we covered prevent any temperature pattern or preference from being detected. Overall, our results show the key role of the position of the front, rather than values of the measured environmental parameters per se, as an explanation for the abundance and distributions of M. atlantica and A. hemistoma. In addition, the topography of the area, with the presence of a submarine canyon, seems to have affected the observed distribution patterns. The presence of the Palamós submarine canyon has been reported to modify the circulation in the area, inducing a shelfward deflection on the upstream side of the canyon and an offshore flow on the downstream side (Alvarez et al. 1996Alvarez A., Tintoré J., Sabatés A. 1996. Flow modification and shelf-slope exchange induced by a submarine canyon off the northeast Spanish coast. J. Geophys. Res. 101: 12043-12055., Jordi et al. 2005Jordi A., Orfila A., Basterretxea G., et al. 2005. Shelf-slope exchanges by frontal variability in a steep submarine canyon. Prog. Oceanogr. 66: 120-141.). In relation to these shelf-slope exchanges, high abundances of both species were observed on the canyon edges, particularly when the shelf-slope front intersected the canyon mouth (mid-May and late June surveys).

In summary, the shelf-slope front was the main factor controlling the abundance and distribution of the two most abundant and representative species of planktonic cnidarians in the NW Mediterranean, the siphonophore M. atlantica and the hydromedusa, A. hemistoma. A high degree of coupling was observed between the short timescale variability of the front’s location and the spatio-temporal distributions of the species. The front seemed to act as a barrier preventing their offshore displacement, as was reflected by the fact that the bottom depth and salinity among the analysed variables best explained the distributions and abundances. The strong hydrographic variability associated with shelf-slope fronts largely determines the seasonal and interannual variability of gelatinous zooplankton and their predation impacts on the planktonic community in this region.

AcknowledgementsTop

The authors wish to thank our friend Dr. Francesc Pagès, who passed away on 5 May 2007, for his teaching. This study began with Francesc and the authors have finished it as a tribute to him. Special thanks go to Dr. A. Canepa and S. Soto for their inestimable help with the statistics and GIS, respectively, and to Charlie Miller for the English revision. This study was partially supported by the EU Project VECTORS (FP7 OCEAN-2010, 266445) and the Spanish project FISHJELLY (MAR-CTM2010-18875). This study is a contribution of the Marine Biodiversity Conservation Group (MEDRECOVER) 2014SGR-1297 and the Ecology of Marine Communities Group (2014SGR-1364) at the Institut de Ciències del Mar-CSIC.

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