Deep-sea suprabenthos assemblages (Crustacea) off the Balearic Islands (western Mediterranean): Mesoscale variability in diversity and production

J.E. Cartes; V. Mamouridis; E. Fanelli

Journal of Sea Research 65 (2011) 340–354 Contents lists available at ScienceDirect Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s Deep-sea suprabenthos assemblages (Crustacea) off the Balearic Islands (western Mediterranean): Mesoscale variability in diversity and production J.E. Cartes ⁎, V. Mamouridis, E. Fanelli Institut de Ciencies del Mar, CSIC, P.g Maritim de la Barceloneta, 37-49 08003 Barcelona, Spain a r t i c l e i n f o Article history: Received 3 September 2010 Received in revised form 20 January 2011 Accepted 3 February 2011 Available online 18 February 2011 Keywords: Suprabenthos Western Mediterranean Diversity Production a b s t r a c t The composition of suprabenthic crustacean assemblages, their diversity, production (P) and production/ biomass (P/B) ratios, were analyzed at species level along two transects situated to the north (N) and south (S) of Mallorca (Balearic Islands, western Mediterranean) at depths between 134 m and 760 m, based on a ca. bi-monthly sampling performed between August 2003 and June 2004. Differences with depth and season in assemblage composition and diversity were analyzed as a function of the contrasting environmental features (e.g. water mass dynamics) of the two areas. We identiﬁed 187 species (18 decapods, 5 euphausiids, 16 mysids, 76 gammaridean amphipods, 13 hyperiids, 1 caprellid, 21 isopods and 37 cumaceans). Substantial mesoscale variability in the deep-sea suprabenthic assemblages coupled with diversity trends between the N and S transects were found. Seasonality was the most important gradient inﬂuencing the dynamics of suprabenthos over the upper (350 m) and middle (650–750 m) slope in the N area. Conversely, the S area appeared to be more stable temporally with depth as the main gradient inducing assemblage differences. Different depth-related patterns were observed both for diversity and P/B. To the north diversity was very low at the shelf-break, increasing on the upper-slope (H′ N 3.00) and then decreasing again on the middle-slope. To the south diversity increased smoothly downward, reaching the highest values on the middle-slope. Regarding productivity, P/B was highest at intermediate depths to the north (over ca. 450–500 m), while to the south highest P/Bs were found deeper (over ca. 600–650 m). The higher P/B at intermediate depths found along N are likely due to higher % of organic matter (OM) in sediments, a product of oceanographic frontal systems. In particular, P/B was higher along N among omnivores and detritus feeders (e.g. Andaniexis mimonectes, Lepechinella manco and combined cumaceans), coupled to enriched OM in sediments, while along S mesoplanktonic carnivores (Rhachotropis spp.) had higher P/Bs. We conclude that on the north slope the inﬂuence of frontal systems and more active ﬂow dynamics of different water masses (WIW and LIW) increases natural disturbance in the area, increasing productivity and diversity of suprabenthic peracarids in the Benthic Boundary Layer. Also, species showed a displacement of their average distributions (their Centres of Gravity, CoG) to shallower depths along N, which is another indicator of more favorable habitat conditions for suprabenthos in the 400–500 m range at N. © 2011 Elsevier B.V. All rights reserved. 1. Introduction The Benthic Boundary Layer (BBL) is a transitional zone (ecotone or ecocline) between pelagic and benthic domains (Dauvin and Vallet, 2006) occupied by a diverse community composed of vagile megafauna (e.g. ﬁshes and large decapod crustaceans) and small swimming macrofauna (mainly peracarid crustaceans, copepods, eucarids and gelatinous taxa). The swimming macrofauna constitute the suprabenthos (=hyperbenthos) (Brunel et al., 1978). While the megafauna have a wider distribution both in the water column and in benthic domains, the deep-sea suprabenthos is highly diversiﬁed ⁎ Corresponding author. Tel.: +34 932309500; fax: +34 932309555. E-mail address: jcartes@icm.csic.es (J.E. Cartes). 1385-1101/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2011.02.002 within the BBL (especially peracarids), and it must be adapted to live in that interface (ca. between 0 and 2 m above the bottom). Suprabenthos has an important trophic role in deep-sea ecosystems as prey of important megafaunal species, (e.g. target species of ﬁsheries, such as M. merluccius and Aristeus antennatus) (Cartes et al., 2001). Suprabenthic crustaceans (e.g. amphipods and cumaceans), occupy 2–3 trophic levels with some species exploiting detritus and others being carnivores on meiofauna and small zooplankton (Madurell et al., 2008; Fanelli et al., 2009a,b). Therefore, its exploitation of particulate organic matter (POM) and its role as prey make it a non-trivial compartment in the function of deep-sea trophic webs (Cartes et al., 2001). Suprabenthos are especially important in the diet of juvenile ﬁsh and decapods (Cartes et al., 2008a) and of ﬁsh in the Mediterranean below 1000 m (Carrassón and Cartes, 2002). Seaﬂoor dynamics have repeatedly been suggested to be affected by cyclic food availability, particularly periodic phytodetritus deposition J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 (vertical ﬂux: Billett et al., 2001) and by advective ﬂuxes in areas with mainland inﬂuence (e.g. via submarine canyons: Cartes et al., 2009a). Depth, seasonality and latitude are often the main gradients determining spatial and temporal changes in marine communities (Corliss et al., 2009; Rombouts et al., 2009), with the spatial (e.g. regional and global) and temporal scales adopted in such analyses being crucial (Watts et al., 1992; Crame, 2000). Latitudinal gradients, for instance, are important determinants of species richness in terrestrial ecology. By contrast the inﬂuence of latitude on diversity seems to be less consistent in marine environments (Rex et al., 2000), especially for some benthic taxa forming regional hotspots of diversity (Crame, 2000; Rombouts et al., 2009). Gradients such as depth or latitude are associated with an array of different environmental variables (e.g. water temperature [T]; salinity [S]; proportion of organic matter [OM] — see Cartes et al., 2008b; sediment grain size; and dissolved oxygen — see Dickinson, 1978) that act directly on organisms, inﬂuencing the distribution and diversity of species (e.g. in the case of planktonic copepods: Rombouts et al., 2009). Diversity patterns of benthos also can be related with latitudinal gradients at large spatial scales (Rex et al., 1997). At more local scales, spatial and temporal changes in biomass peaks of benthic species living at great depths have been related with highly productive zones and episodes (Billett et al., 2001 and Ruhl and Smith, 2004 in the abyss; Cartes et al., 2009a on the slope). Hypotheses have been proposed to explain trends in deep-sea species diversity. They relate to the stability of environments, to production rates and to predation pressure by the highest trophic levels (Gage and Tyler, 1991; Rex and Etter, 2010). However, exactly how diversity relates to environmental conditions or to local productivity is unknown for the deep sea, because of the lack of appropriate data sets (Corliss et al., 2009). Suprabenthos are a vagile part of benthos, not quantitatively sampled with box-corers. However, these organisms are subject to gradients similar to those affecting benthos. Assemblage composition of deep-sea suprabenthos has mainly been related to depth (e.g. Western Mediterranean: Bellan-Santini, 1990; Cartes and Sorbe, 1993, 1997, 1999a; Cartes et al., 2003; Atlantic: Marques and Bellan-Santini, 1987; Brandt, 1995; Dauvin and Sorbe, 1995; Sorbe, 1999). Environmental coupling is well documented for shallow water species and communities, even at shelf-slope breaks (Joselson and Conley, 1997; Richoux et al., 2004). By contrast, the interaction between chemical and physical variables and assemblage dynamics of deep-sea suprabenthos has scarcely been studied (Elizalde et al., 1999; Cartes et al., 2008b), particularly at species level. Small-scale spatial variations among suprabenthic assemblages are poorly known, although some differences in the composition of species and trophic guilds between mainland and insular areas have been described (Cartes et al., 2009b). Even in stable environments such as deep-sea areas, spatial differences (e.g. in terms of biomass) among benthos can reach more than an order of magnitude between neighboring areas, which is often discussed in terms of differences in food supply (Dickinson and Carey, 1978; Lampitt et al., 1986). The biological cycles of deep-sea invertebrates have repeatedly been linked with cyclic food availability, often associated with periodic phytodetritus deposition (vertical ﬂux: Richoux et al., 2004), less often to advectiveterrigenous ﬂuxes in areas with mainland inﬂuence (e.g. via submarine canyons: Buscail et al., 1990; Cartes et al., 2009b). Populations of marine species can occupy patches of high quality habitat, and they can exist as a number of metapopulations that may have limited exchange of individuals among them (Jacob and Sale, 2006), hence the importance of comparative studies at short and mesoscale levels. In shallow waters, local changes in environmental quality (e.g. food supply) may affect secondary production of species at short spatial scales (Cartes et al., 2009c). In this study, the dynamics of suprabenthos have been simultaneously analyzed at a mesoscale in two areas around the Balearic Islands (in the North-West and South of Mallorca) in relation to 341 environmental dynamics (see Cartes et al., 2008b). The two areas have different oceanographic conditions related with dynamics of water masses (López-Jurado et al., 2008) and primary production (Cartes et al., 2008b). In the Balearic Basin, the mainland slope off the Catalonian coast, could be deﬁned as a hotspot of diversity with a substantial set of peracarid crustaceans newly described since the 1990 s (Cartes and Sorbe, 1997, 1999a; Jaume et al., 2002; Ruffo et al., 1999; San Vicente and Cartes, 2011). The Balearic Basin has the structure of a large submarine canyon, with differences between the mainland and insular slopes. For example, there are substantial variations in megafaunal depth distributions and assemblages (Cartes et al. 2009b). Differences in the current regime, in river discharges and in advective downward transport of POM may contribute to these faunal distinctions. In contrast, the ecology of suprabenthos on the insular slope has not been studied in detail (Cartes et al., 2003). While most current deep-sea research remains descriptive with exploratory objectives, and focuses at large geographic scales in search of hotspots of diversity, the aim of this study is to examine relationships among suprabenthic peracarid diversity and dynamics of environmental variables at a mesoscale level. We have compared two adjacent areas with different environmental conditions. Our speciﬁc objectives are: 1) to describe the main gradients responsible for spatio-temporal changes in suprabenthos assemblages distributed in adjacent areas, examining mesoscale differences between assemblages; 2) to compare trends in the distribution of diversity between the slopes to the northwest and to the south of Mallorca; and 3) to compare patterns of production (P and P/B ratios) between species inhabiting these two contrasting areas and explore whether the observed production differences are a function of environmental variability (water mass dynamics and local sea-surface productivity). 2. Materials and methods 2.1. Study area The study was carried out in two areas (sampling transects) around Mallorca (Balearic Islands: western Mediterranean). Sampling was an aspect of the IDEA project (Fig. 1). One area was located on to the north (indicated as N: 38°98′ N–2°57′ E; 39°14′ N–2°76′ E), and the other to the south of the island of Mallorca (indicated as S: 39°68′ N–2°18′ E; 39°81′ N–2°37′ E) with a ca. 600 m minimum depth separating both areas in the Mallorca channel, between the islands of Mallorca and Eivissa (Cartes et al., 2008b). The N area is close to the harbor of Sóller, adjacent to the Balearic sub-basin (between the northeast coast of the Iberian Peninsula and the Balearic Islands). This area is characterized by a narrow shelf and a slope that descends sharply, when compared to the S site. In general, we found higher water column variability at the north transect (López-Jurado et al., 2008). The differences in environmental conditions between N and S Mallorca are related with mesoscale hydrographic features: at N the occurrence of the Western Mediterranean Intermediate Water (WIW) and strong winds generate high variability of environmental factors such as salinity and temperature (LópezJurado et al., 2008). The S area is close to the Cabrera Archipelago and included in the Algerian sub-basin. There the shelf is ﬂat and the slope descends gently; oceanographic variability at S is governed by eddies detaching from the Algerian current. 2.2. Sampling design and data collection 2.2.1. Biological data Suprabenthos were sampled at four different depths (approximately over 150 m, 350 m, 650 m and 750 m) on both transects, a range including the shelf-break and the upper and middle slope. A total of 46 suprabenthos sledge hauls were performed during six cruises. All samples were taken during daytime on 3–7 August 2003, 342 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 Fig. 1. Map of the two study areas (circles) around the Island of Mallorca, with stations (•) situated over 150, 350, 650 and 750 m. Arrow indicates the position of the front generated by the Balearic current ﬂowing along the northwestern slope of the Island (from López-Jurado et al., 2008). 25 September–1 October 2003, 13–21 November 2003, 14–20 February 2004, 7–13 April 2004 and 23–28 June 2004. In two cruises, two stations situated off Sóller (IDEA1103: 750 m; IDEA0204: 150 m), could not be sampled due to bad weather conditions. Suprabenthos were sampled with a Macer-GIROQ sledge, equipped with two superimposed nets with mouth openings between 10–40 cm and 50–90 cm above the bottom. Only the lower net samples, in which the largest amounts of fauna were found, were processed (see Cartes et al., 2008b for further details on the methodology). One haul was taken at each station because previous studies using sledges had shown that one haul was enough to characterize the community of suprabenthos for a particular area/ time (Brattegard and Fossa, 1991). The sledge nets have 500 μm mesh openings and were trawled at ca. 1.5 knots. The durations of sledge hauls over the bottom were ca. 10 min. Both vessel speed times haul duration and ﬂowmeter readings (attached to net mouths) were used to estimate the area of samples for standardizing abundances (individuals/100 m2). Specimens were immediately sorted with the help of forceps and frozen on board at −20 °C (for later stable isotope analyses). Sorting was completed in a laboratory (sometimes of aliquots ranging from 1/2 to 1/8 of samples for the abundant smaller organisms, primarily copepods and ostracods). Animals were identiﬁed to the lowest possible taxonomic level under a stereomicroscope (at ×10–×40), with peracarids and eucarids identiﬁed to species and counted for statistical analyses. hauls collecting megafaunal ﬁsh and invertebrates at the same stations (see López-Jurado et al., 2008; Moranta et al., 1998, for details). Temperature at the surface (Tsur) and temperature and salinity at 5 m above the bottom (T5mab; S5mab) were measured. Sediment for granulometric and organic analyses were collected using a Shipeck grab. Sediment variables considered were the mean grain size (phi, in micrometers) and percentage of mud (see Cartes et al., 2008b, for more details). Total organic matter content (%TOM) of collected sediment was calculated as the difference between dry weight (DW: 80 °C during 24 h until reaching constant weight) and ash weight (500 °C in a furnace during 2 h). Phytoplankton pigment concentrations (ppc, in terms of mg Chl a m−2) were obtained from http://reason.gsfc.nasa.gov/Giovanni, and used as indicators of the availability of food resources at the lowest levels of the trophic chain. Monthly average ppc values were used for the positions where the sledges/plankton net samples were taken. Data were from different periods: simultaneously, 1 and 2 months before samplings (indicated in the text as Chlasim, Chla1mo and Chla2mo). Among selected variables, those recorded at the surface and not depthdependent (Tsur, Chl a) can be considered as seasonally dependent variables. Depth-dependent variables (the rest) were taken on or over the bottom at sampling stations ranging between 150 and 750 m depths. 2.2.2. Environmental data Environmental data were collected for all stations and surveys. CTD transects (SBE911 and SBE25 proﬁlers, and SB37-SM mounted on the mouth of a bottom trawl) were performed simultaneously with Analyses were focused on suprabenthic species of peracarid and eucarid crustaceans excluding all non-swimming species/taxa (see Annex 1). Thus epibenthic and infaunal species (e.g. Munida tenuimana within Decapods, Tanaidacea, and Pycnogonida) and taxa 2.3. Data analyses J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 that are not peracarids or eucarids were not included in the multivariate analysis. Species/taxa appearing less than twice in hauls were removed from the data matrix, as were data from station IDEA0604 off Soller at 150 m depth that lacked any peracarids and eucarids. Nonparametric Multidimensional Scaling (nMDS; Clarke et al., 1993) was performed, using the Spearman Rank Correlation as a distance measure, to visualize multivariate abundance patterns. Principal factors to bear in mind to explain the ordination of hauls were depth, area and season. seasonality was expressed either as Factor Season (Winter — November and February, Spring — April, Summer — June and August and Autumn — September) or as months for statistical analyses; in a second step we contrasted periods of water column homogenization (November, February and April) vs stratiﬁcation (June, August and September). Distance-based permutational multivariate analysis of variance (PERMANOVA, Anderson et al., 2008) was used to test three null hypotheses of no differences among the suprabenthic assemblages: i) between the two areas (N vs S), ii) among the four depths within each area and iii) among the four sampling seasons. The experimental design has three factors: area (with two levels), depth (with four levels, nested in area) and season (with four levels and crossed with area and depth). All factors were ﬁxed. The same distance matrix was used as implemented in the nMDS. Permutation of residuals under a reduced model was used as the permutation method (maximum number of permutations = 9999), because of its good empirical results in giving the maximum discriminant power (Anderson and Legendre, 1999; Anderson and ter Braak, 2003). For each Pseudo-F test, and post-hoc tests for signiﬁcant effects are also reported. Two-way SIMPER analyses (Clarke, 1993) were performed on the Bray–Curtis distance of standardized data (N individuals/100 m2) in order to identify species contributions in terms of abundance. Factors compared were depths (grouping the hauls at 650 and 750 m) and areas. Species diversity (H′, Shannon–Wiener index using loge) and number of species (S) were also calculated for each depth stratum, and depth-related trends were analyzed for N and S Mallorca areas. Principal components analysis (PCA, based on Euclidean distances) was used for N and S separately, producing ordinations of stations (all depths and months) in a space with axes deduced by the reduction of the information given by environmental variables to two principal components explaining the variance of the system. These ﬁrst components are typically correlated with some of the observed variables. The relationships between species assemblage structure and existing environmental gradients were tested by means of nonparametric Spearman rank correlations between nMDS dimensions of species abundance data and environmental variables simultaneously recorded. Centres of Gravity (CoG, Stefanescu et al., 1992) indicating the optimal habitat of species, which are often located where the species also reach their maximum density, were calculated for abundances of the identiﬁed peracarids (see Cartes et al., 2009a). Calculations were done separately for N and S transects off Mallorca. Tests were performed comparing the two areas. We performed the analysis on suprabenthic peracarid species, which are well sampled with the sledge, excluding pelagic taxa (decapods, euphausiids and hyperiids). All statistical analyses were performed by using PRIMER6 and PERMANOVA + (Anderson et al., 2008; Clarke et al., 1993) and STATISTICA 7.0. 2.4. Secondary production estimates For dominant species found in the study areas, seasonal trends in abundance were analyzed to establish their basic life cycles and determine cohort production intervals for P and P/B calculations by 343 the Hynes-Hamilton or size-frequency method (Hynes and Coleman, 1968; Menzies, 1980). The calculations provided estimates of annual secondary production for peracarid species. Demographic categories of eucarids with planktotrophic larvae were not fully sampled with the suprabenthic sledge and were not considered for P and P/B calculations. Estimation of P (and P/B) involves calculation of an annual average length-frequency distribution (the mean annual cohort) from quantitative samples taken at evenly spaced intervals throughout the year. Production is then estimated as the sum of the losses of individuals from one size class to the next plus the biomass loss, compensated by the increase in mean individual weight with increasing age (Cartes and Sorbe, 1999b, Mees and Jones, 1997). The method is applied when it is not possible to identify and follow the growth/mortality of single cohorts through time, and it assumes linear growth patterns. Therefore, this method is suitable for shortlived and fast-growing species, such as those characteristic of suprabenthos. The following formula was used (Hynes and Coleman, 1968): " # qﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃﬃ 12 P = i⋅ ∑ dj −dj + 1 ⋅ bj ⋅bj + 1 ⋅ CPI j=1 i−1 where i is the number of size classes represented in the average length-frequency distribution, dj and bj are the density (ind m−2) and the biomass (g WW m−2), respectively, of the jth size class in the average length-frequency distribution and CPI is the cohort production interval (months) (Cartes and Sorbe, 1999b, Mees and Jones, 1997). Specimens belonging to dominant species at N and S transects off Mallorca were measured under a stereomicroscope (at ×10–×40 depending on the species) with the help of an ocular micrometer. Mean annual biomass (B) of each species was calculated as the sum of the biomass of all size classes (bj) in the average lengthfrequency distribution (Cartes and Sorbe, 1999b). For each species production/biomass ratio (P/B, productivity) was calculated as a standardized measure allowing comparisons among species having different individual biomass (Plante and Downing, 1989). Determining the cohort production interval requires a basic knowledge of species life histories. In our study, CPI was taken when possible from data on the abundance of oostegal females and peaks of abundance of juveniles in the investigated areas, or from existing literature (e.g. Cartes and Sorbe, 1999b). Nevertheless, P/B can vary depending on latitude and geographic area. In any case, because our objective was a comparison of P and P/B between two nearby areas, rather than accurate estimation of secondary production, we consider the adopted/assumed estimates of CPI to be sufﬁciently valid. Differences in secondary production (P) and P/B between the two areas at N and S of Mallorca were analyzed. The relative differences in production (R index) were calculated according to the following formula (Collie et al., 2000): %Diff = ðPN −PS Þ ⋅100 PS where PN and PS are the secondary production at the N and S of Mallorca, respectively. Differences in P/B ratio between N and S (P/BN − P/BS) were estimated as well. Wilcoxon Sign Rank Test was performed between N and S values of P and P/B considering all taxa together and species grouped by taxon (mysids, amphipods and cumaceans). Tests on isopods were not performed because there were only a few species. P and P/B of peracarid species were plotted against their optimal depth distributions (CoG) for the N and S transects, in order to compare depth-related trends between the areas. 344 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 Fig. 2. MDS ordination for all samples. Labels indicate the sampling area (N: Northwest and S: South) around Mallorca. Symbols indicate the mean depth of each sledge haul (Δ = 150 m; ∇ = 350 m; □ = 650 m; and * = 750 m). 3. Results 3.2. Assemblage structure 3.1. Species composition An overall nMDS showed three well-deﬁned assemblages, separated by depth ranges: samples taken at 150 m, 350 m and 650–750 m were clearly segregated from each other (Fig. 2). An nMDS performed separately for each bathymetric range (Fig. 3a–c) indicated a grouping or separation of samples from 350 m and 650–750 m by the condition of the water column (homogeneized in February, April and November vs stratiﬁed in June, August and September). In the deepest range, hauls were separated under the criterion of homogenized vs stratiﬁed only on the N transect (Fig. 3d). PERMANOVA were statistically signiﬁcant for all factors analyzed (Table 1a). Hauls (species composition or assemblages) at each depth range differed from those at the other depths, except those at 650 and 750 m that were statistically similar. Species composition differed by A total of 18540 peracarid and 323 eucarid specimens were identiﬁed in our sampling. The complete list with depth range inhabited by species/taxon to the N and S of Mallorca and with average abundances within the depth range is in Annex 1. Specimens identiﬁed belong to 187 species/taxa: 18 species of Decapoda, 5 of Euphausiacea, 16 of Mysidacea, 76 of Amphipoda Gammaridea, 13 of Hyperiidea, 1 Caprellidea, 21 of Isopoda and 37 of Cumacea. The centres of Gravity (CoG) of peracarid species were calculated and plotted against P and P/B (see Section 3.7). The Wilcoxon test showed evidence of signiﬁcantly deeper values of CoG in the S than in the N (V = 5, p b 0.001). Fig. 3. MDS ordinations of samples from a) Shelf-break (150 m); b) Upper-slope (340 m); c) Middle-slope (650–750 m); d1) Middle-sloe of N and d2) Middle-slope of S. Labels indicate Area (N = Northwest and S = South) and month (2 = February; 4 = April; 6 = June; 8 = August; 9 = September; and 11 = November); ∇ = homogeneity and ○ = stratiﬁcation of the water column. 345 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 Table 1 PERMANOVA based on Spearman's rank correlation distance matrix of a) the whole dataset, b) hauls on S transect and c) hauls on N transect. Tests were done by pairwise comparisons only between contiguous periods (only signiﬁcant tests reported). Source a) Total Area Depth(area) Season Res Total b) South Depth Season Res Total c) North Depth Season Res Total ns: not ⁎⁎⁎ ⁎⁎ ⁎ df MS Pseudo-F 1 6 566720 569920 8.68⁎⁎⁎ 8.73⁎⁎⁎ 3 34 44 310170 65288 4.75⁎⁎ 3 4 16 23 46856 9163 6574 7.13⁎⁎⁎ 1.39 ns 3 4 13 20 25406 9194 2470 10.28⁎⁎⁎ 3.72⁎ Pairwise N≠S 150 ≠ 350 ≠ 650 = 750; 650–750 N ≠ 650–750 S Spr = Sum ≠ Aut = Win = Spr 150 ≠ 350 ≠ 650 = 750 150 ≠ 350 ≠ 650 = 750 Spr = Sum ≠ Aut ≠ Win = Spr signiﬁcant. p b 0.001. p b 0.01. p b 0.05. season only between those hauls collected in summer and autumn. Pairwise tests performed among depth strata (150, 350 and 650– 750 m) showed signiﬁcant differences for species composition at both N and S transects. PERMANOVAs computed for each area showed signiﬁcant differences among depths in both areas; however, there was a signiﬁcant effect of season only along the N transect: summer, autumn and winter assemblages there were all distinctive (Table 1b–c). As conﬁrmed by SIMPER analyses, different species typiﬁed each bathymetric assemblage (Table 2a) and typiﬁed the N and S areas (Table 2b). Diversity was low at the shelf-break stations on both transects, which were inhabited by a few mysid and amphipod species. The upper and middle slope assemblages were less strongly dominated, with contributions to similarity among samples more evenly distributed among species. On the upper slope the most abundant species were Hemilamprops normani, Boreomysis megalops and Rhachotropis integricauda. Munnopsurus atlanticus and Boreomysis arctica were the dominants on the middle slope. The N and S areas differed mainly in the increasing contribution of M. atlanticus in the S and the high abundance of Nematoscelis megalops in the N. A few species were observed almost exclusively in the N, such as Primno macropa and some other hyperiids. 3.3. Diversity patterns Two different diversity patterns were observed in relation to depth (Table 3). In both areas the lowest value of H′ was observed at the shelfbreak, and it was greater on the slope. However, diversity at N was very low at the shelf-break, increasing on the upper-slope (H′ N 3.00) and then decreasing again on the middle-slope. At the S transect diversity increased smoothly, reaching the highest values on the middleslope. One-way ANOVA showed signiﬁcant differences in diversity both at the North transect (for H′: F 3, 21 =19.62; p=3·10−5; for S′: F 3, 21 = 11.58; p=3·10−4), and at the south transect (for H′: F 3, 24 =3.58; p=0.04; for S: F 3, 24 =5.69; p=0.01) areas. Paired comparisons (Tukey tests) between depth strata showed signiﬁcant differences at North among all depth strata, both for H′ (shelf-break vs upper slope: p = 10−5; upper slope vs middle slope: p =0.01) and for S (shelf-break vs upper slope: p = 4 · 10−4; upper slope vs middle slope: p =0.01). By contrast, along the South transect Tukey tests were not signiﬁcant when H′ and S were compared between contiguous depth strata. Table 2 Results of two-factor SIMPER analysis based on Bray–Curtis similarity (cut-off at 80%). a) Factor depth Species Shelf break (av. Sim.: 11.66) Leptomysis gracilis Primno macropa Anchialina agilis Westwoodilla rectirostris Hyperia schizogeneios Campylaspis glabra Phronima sedentaria Gnathia sp. L Disconectes furcatum Upper slope (av. Sim.: 27.80) Hemilamprops normani Boreomysis megalops Rhachotropis integricauda Campylaspis sulcata Gnathia sp. L Campylaspis glabra Procampylaspis armata Lepechinella manco Anchialina agilis Scopelocheirus hopei Ilyarachna longicornis Monoculodes packardi Bathymedon longirostris Westwoodilla rectirostris Ileraustroe ilergetes Disconectes furcatum Munnopsurus atlanticus Lophogaster typicus Rhachotropis grimaldii Rhachotopis caeca Middle slope (av. Sim.: 30.66) Munnopsurus atlanticus Boreomysis arctica Rhachotopis caeca Bruzelia typica Nematoscelis megalops Rhachotropis rostrata Gnathia sp. L Tryphosites longipes Syrrhoe afﬁnis Ilyarachna longicornis Andaniexis mimonectes Rhachotropis grimaldii Nicippe tumida Tryphosites alleni b) Factor area Contrib % 13.27 13.07 11.36 11.04 10.76 7.24 4.90 4.82 4.77 11.88 11.81 9.32 7.09 5.25 5.24 4.24 2.79 2.78 2.64 2.25 2.08 1.98 1.88 1.83 1.81 1.71 1.61 1.55 1.42 22.60 17.17 9.27 4.99 4.37 3.37 3.32 3.17 3.14 2.58 1.99 1.82 1.40 1.35 Species North (av. Sim.: 24.76) Boreomysis arctica Munnopsurus atlanticus Nematoscelis megalops Rhachotopis caeca Gnathia sp.L Bruzelia typica Hemilamprops normani Rhachotropis grimaldii Campylaspis glabra Campylaspis sulcata Tryphosites alleni Rhachotropis rostrata Syrrhoe afﬁnis Ilyarachna longicornis Stegocephaloides christianensis Primno macropa Hyperia schizogeneios Procampylaspis armata Gennadas elegans Scopelocheirus hopei Bathymedon longirostris South (av. Sim.: 30.29) Munnopsurus atlanticus Boreomysis arctica Rhachotopis caeca Tryphosites longipes Bruzelia typica Boreomysis megalops Rhachotropis rostrata Ilyarachna longicornis Gnathia sp. L Syrrhoe afﬁnis Rhachotropis integricauda Andaniexis mimonectes Procampylaspis armata Belonectes parvus Paramblyops rostrata Campylaspis glabra Westwoodilla rectirostris Bathymedon longirostris Platysympus typicus Leptomysis gracilis Camylaspis verrucosa Contrib % 13.77 10.22 8.04 7.09 5.14 4.96 4.88 2.86 2.83 2.70 2.27 2.10 1.99 1.93 1.89 1.73 1.62 1.51 1.43 1.41 1.40 22.72 13.01 7.64 4.07 3.20 2.99 2.99 2.90 2.83 2.72 2.50 2.39 1.58 1.45 1.38 1.35 1.34 1.28 1.16 1.16 1.13 No signiﬁcant differences were found comparing mean H′ values of north with south samples from any depth range (Table 3). Also, the number of species showed the same trend as described for H′ (Table 3). 3.4. Seasonal trends in species abundance Abundance of dominant species showed similar seasonal trends in each bathymetric assemblage (Fig. 4). The distribution of species abundances did not differ statistically (Kolmogorov–Smirnov test: p N 0.1) comparing N and S areas, so species abundances for N and S were plotted together. At the shelf-break, all dominant (in abundance) species presented a single peak in abundance in summer (June–August). On the upperslope, most species showed two evident peaks, in spring (April) and late summer (August). This was observed in two amphipods (Rhachotropis integricauda and Lepechinella manco), in the isopod Disconectes furcatum and in Hemilamprops normani, Campylaspis sulcata and Campylaspis glabra, the last being especially abundant in August. Two mysids showed a similar pattern, with the higher peak of 346 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 Table 3 Trends of diversity. H′ (Shannon–Wiener index), S (number of species), expressed as mean ± C.I. (95%) with number of hauls (n) for each bathymetric assemblage and total values, respectively in the north (N) and south (S) areas. more dominant species also peaked in abundance during winter (February), e.g. Boreomysis arctica and Munnopsurus atlanticus. H′ S n 3.5. Environmental conditions of N and S Shelf-break Upper-slope Middle-slope Total 1.55 ± 0.29 3.23 ± 0.14 2.54 ± 0.28 2.55 ± 0.30 8.00 ± 3.58 57.83 ± 8.96 31.54 ± 11.18 34.57 ± 9.96 4 6 11 21 Shelf-break Upper-slope Middle-slope Total 2.23 ± 0.17 2.42 ± 0.4 2.81 ± 0.26 2.57 ± 0.2 16.67 ± 4.66 39.5 ± 16.86 46.75 ± 10.07 37.42 ± 8.46 6 6 12 24 In PCA biplots for both N and S we can identify depth and seasonal gradients linked to some groups of hauls (Fig. 5). At N the ﬁrst two principal components of the PCA explained 43.7% and 27.8% of the total variance, respectively. The main variables correlated with the ﬁrst component were Chlorophyll a (Chlasim, Chla1mo and Chla2mo) and in the opposite direction Tsur, both of which are season-related variables (and not depth-dependent because they are recorded always at surface). The second component was linked to S5mab and % mud and in opposite direction median phi. April and February samples grouped together in the biplot, mainly related to Chl a readings, while August and September hauls grouped together related with (higher) Tsur. At S the ﬁrst two principal components explained 38.3% and 30.0% of the total variance. The ﬁrst component depended more on median phi and Chla1mo and in the opposite direction on S5mab and Tsur. The second component depends more on % mud and Chlasim. In contrast N S abundance in August (Boreomysis megalops and Lophogaster typicus), while one species of amphipod (Schopelocheirus hopei) showed a more unimodal pattern, being especially abundant in April. On the middle-slope, species showed weaker ﬂuctuations through the year in comparison to the shallower depths. The highest abundances of several species were observed in summer (June–August), and the Fig. 4. Mean abundances (ind/100 m2) of the most abundant species during the sampling period. 347 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 including all hauls from the two areas, was correlated with depth and chemical–physical variables of both water and sediment (e.g. S5mab and OM%) and Dimension-2 correlated with T5mab. Different patterns were found in each depth assemblage (Table 4). At the shelf-break no signiﬁcant correlations were found; on the upper-slope Dimension-1 was correlated with Tsur, Chlasim and %OM. On the middle-slope Dimension-1 was correlated with S5mab and median phi. At N Dimension-1 was correlated with different water column variables (T5mab and S5mab and Tsur). At S Dimension-1 was correlated with sediment-related variables such as %mud and median phi. 3.7. Secondary production Fig. 5. Principal component analysis (PCA) ordination for the environmental variables recorded on a) N of Mallorca and b) S of Mallorca Labels indicate month (Feb = February; Apr = April; Jun = June; Aug = August; Sep = September; and Nov = November). Symbols indicate depth range (Δ = Shelf-break; ○ = Upper-slope; and ∇ = Middle-slope). to N, the environmental conditions were linked both to depth and seasonal gradients. 3.6. Correlations between MDS dimensions and environmental variables Dimensions of the nMDS were signiﬁcantly correlated with a number of the environmental variables explored (Table 4). Dimension-1, A total of 18,380 individuals were measured to estimate production and P/B for 30 target species in the two studied areas, together with W (mean individual weight, Biomass/Density) and CPI (Table 5). CPI was assumed to be the same in both N and S populations given the relative proximity of the two areas. Production varied between 1 · 10−5 mgWW m−2 year−1 for Disconectes furcatum and 10.5 · 10−2 mgWW m−2 year−1 for Boreomysis arctica (both at N). The P/B ratios were between 3.3 for Lophogaster typicus and 12.1 for Andaniexis mimonectes (the ﬁrst in S, the second in N). Out of 30 species considered, 18 showed higher production estimates at S rather than at N (Fig. 6). Among amphipods 11 had higher values at S and only 3 at N. All isopods had higher values at S, while among mysids there was no evident trend. Among cumaceans, the trend was 4 higher values at N and 2 at S. An opposite trend was observed in P/B values (Fig. 6): 18 species showed higher P/B values at N and 12 species at S. Many mysid and isopod species showed higher values at N as well as all cumaceans. On the contrary, among amphipods a majority of species showed higher values at S (9 species) than at N (5 species; Fig. 6). The Wilcoxon Signed Rank Tests performed to compare P and P/B values between the two areas were not signiﬁcant (P: V=141, p= 0.924; P/B: V = 309, p = 0.059) considering all taxa. Testing each taxon separately showed signiﬁcant p-values between N and S production for amphipods (PS greater than PN: V=19, p-value=0.018) and P/B values for cumaceans (P/BN greater than P/B S : V=21, p-value= 0.016). No signiﬁcant p-values were found for mysids. Regarding depth-related trends of suprabenthos production (Fig. 7), P decreased progressively downward in the S area for species with deeper Centres of Gravity (CoG), while at N the distribution pattern of P was not clearly related to depth. In other words, we found the higher values of P at S distributed deeper than at N, though this trend was not signiﬁcant (Mann–Witney test comparing N vs S P values). P/B followed two different patterns, with highest values at intermediate depths along N (over ca. 450–500 m), while at S the highest P/B was found Table 4 Spearman's rank correlations between nMDS dimensions and environmental variables. N: Number of valid cases and r: Spearman's rank correlation. Only signiﬁcant correlations are reported. Total Dim1 T5mab Tsur S5mab O. M. (%) Mud (%) Median phi Chla1mo Chlasim Dim2 T5mab ⁎ p b 0.05. ⁎⁎ p b 0.01. ⁎⁎⁎ p b 0.001. Middle-slope N Middle-slope S Middle-slope N r N Upper-slope r N r N r N r 45 45 45 40 39 40 45 45 − 0.446⁎⁎ – 0.477⁎⁎⁎ 0.457⁎⁎ 0.594⁎⁎⁎ − 0.623⁎⁎⁎ 12 12 12 10 10 10 12 12 – − 0.226⁎ − 0.115 − 0.717⁎ 23 23 23 20 19 20 22 22 – – – – – 0.599⁎⁎ – – 9 9 8 7 7 7 8 8 − 0.733⁎ − 0.783⁎ − 0.867⁎⁎ – – – – – 11 11 11 10 10 10 11 11 – – – – − 0.636⁎ 0.758⁎ 45 0.476⁎⁎⁎ 12 – 23 – 11 – 11 – – – – – – 0.638⁎ – – 348 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 deeper (over ca. 600–650 m) than at N. The mean CoG (±C.I. 95%) at N was 497 ± 30 m and 541 m ± 33 m. Applying a Mann–Witney test comparing P/B at N and S, we obtained signiﬁcant (p = 0.04) differences. Also, 1-way ANOVA showed a signiﬁcant difference at N, comparing the P/B of species for which CoG was b400 m, was between 400 and 500 m and was N500 m (F 2, 30 = 6.75; p = 0.004), with signiﬁcantly higher P/B at 400–500 m (post-hoc Tukey results: b400 m vs 400–500 m: p = 0.004; 400–500 m vs N500 m: p = 0.04). No signiﬁcant differences were found comparing P/B for the same depth groups (F 2, 33 = 0.91; p = 0.41). Highest P/B were found at intermediate depths at N coincided with the highest diversity (both in terms of S and H′) found over the same depth strata (see above). At S we did not ﬁnd such relationship. 4. Discussion The biological diversity of the deep-sea still remains far from reasonably well known (Rex and Etter, 2010; Rex et al., 2000), despite the increasing effort devoted to the study of deep-sea fauna. Suprabenthos in the deep western Mediterranean (Balearic Basin and around the Balearic Islands) constitutes a good example of this. Since the end of the 1980s, when quantitative studies on deep-sea suprabenthos began in the Balearic Basin (Cartes and Sorbe, 1993, 1997; Cartes et al., 2001, 2003), most of the new species described (Jaume et al., 2000; Ruffo et al., 1999; San Vicente and Cartes, 2011) have proved to be relatively abundant and widely distributed in both the western and eastern basins (e.g. Bathymedon longirostris: Madurell and Cartes, 2003; Dactylamblyops corberai: San Vicente and Cartes, 2011). These ﬁndings were possible thanks to the use of the Macer-GIROQ suprabenthic sledge (Dauvin and Lorgeré, 1989) for exploring the deep sediment-water interface (Cartes et al., 1994). The use of suprabenthic sledges has shown that the distribution of deepsea diversity depends not only upon the sampling area covered (Gage and Tyler, 1991) but upon the 3-dimensional distribution of the fauna in the water column, with peracarid crustaceans mainly distributed in the near bottom (0–1.5 m above the sea bed) habitat. Most of these animals escape box-corer sampling (see Cartes et al., 2009c), especially mysids with the highest swimming capacity among deep-sea peracarids. We have found mesoscale variability between deep-sea suprabenthic assemblages and diversity trends in two neighboring zones to the north and south of the Balearic Islands. Seasonality was the most important factor inﬂuencing the dynamics of suprabenthos over the upper (350 m) and middle (650–750 m) slope, especially along the N transect. Conversely, the southern area appeared to be more temporally stable (see below) with depth being the main gradient inﬂuencing assemblage composition. Temporal dynamics of macrofauna (e.g. suprabenthos) have rarely been studied in the deep-sea environment (Cartes et al. 2003, 2008b; Sorbe, 1999), where studies are rather descriptive and focused on scanning wide areas in search of hotspots of diversity. Other studies have not been focused on mesoscale variability but on the depth and large-scale latitudinal gradients in the distribution of diversity (references in Gage and Tyler, 1991; Rex and Etter, 2010). Seasonality near Mallorca at N is conﬁrmed by: i) our evaluation by PERMANOVA of seasonal MDS groups that proved to be signiﬁcant along the entire slope sampled there; ii) our PCA results showing a better temporal segregation of samples at N, with a greater proportion of variance explained (43.7% for the ﬁrst axis); and iii) stronger relationships at N with seasonrelated variables such as Chl a and Tsur. The N and S transects near Mallorca Island exhibit different levels of faunal variability related to the circulation of water masses (López- Table 5 Production (P) and P/B estimates of the 32 target species. N, number of specimens measured; CPI: cohort production interval; W: mean individual weight. North and South correspond to Northwest and South of Mallorca. Species Mysidacea Anchialina agilis Boreomysis arctica Boreomysis megalops Erythrops neapolitana Leptomysis gracilis Lophogaster typicus Mysideis parva Amphipoda Andaniexis mimonectes Bathymedon longirostris Bruzelia typica Illeraustroe ilergetes Lepechinella manco Nicippe tumida Rhachotropis caeca Rhachotropis grimaldii Rhachotropis integricauda Rhachotropis rostrata Stegocephaloides christianensis Syrrhoe afﬁnis Syrrhoites pusilla Westwoodilla rectirostris Isopoda Disconectes furcatun Ilyarachna longicornis Munnopsurus atlanticus Cumacea Campylaspis glabra Campylaspis sulcata Campylaspis verrucosa Diasryloides serrata Hemilamprops normani Procampylaspis armata n CPI North P (mg WW/m2 year) 372 1949 2146 226 95 173 186 12 6.5 12 12 7 12 8 0.00023 0.01517 0.00858 0.00008 0.00052 0.00070 0.00022 512 315 352 275 377 225 815 581 406 427 213 302 132 176 4.5 6.5 6.5 6.5 5.9 7 6.5 6 7 6.5 6 6.2 6.5 7 314 642 1876 482 947 245 177 869 449 12 12 8 7.5 7.3 7.5 5.8 4.7 6.5 P/B W (mg WW/ind) South P (mg WW/m2/year) P/B W (mg WW/ind) 4.07 6.27 4.83 4.90 6.59 5.37 4.65 0.00119 0.01448 0.00405 0.00073 0.02192 0.00617 0.00410 0.00012 0.01360 0.00825 0.00008 0.00162 0.00115 0.00021 3.59 7.11 4.78 4.59 6.00 3.32 4.85 0.00178 0.01040 0.00453 0.00082 0.02538 0.02693 0.00375 0.00010 0.00040 0.00015 0.00002 0.00014 0.00037 0.00070 0.00079 0.00011 0.00078 0.00015 0.00031 0.00028 0.00074 12.11 7.91 6.67 8.25 7.2 6.79 8.15 8.7 10.39 6.26 0.76 6.47 7.72 7.52 0.00028 0.00416 0.00118 0.00018 0.00037 0.00512 0.00183 0.00194 0.00113 0.0057 0.00137 0.00295 0.00175 0.00821 0.00017 0.00070 0.00016 0.00004 0.00006 0.00064 0.00139 0.00036 0.00061 0.00094 0.00014 0.00068 0.00034 0.00086 9.80 8.44 7.19 0.49 6.60 6.48 8.36 8.98 10.80 6.46 7.21 6.52 8.11 8.36 0.00052 0.00313 0.00098 0.00026 0.00033 0.00578 0.00173 0.00184 0.00090 0.00516 0.00160 0.00284 0.00104 0.00443 0.00001 0.00005 0.00071 4.31 4.09 6.81 0.00022 0.00036 0.00186 0.00001 0.00006 0.00195 4.98 4.05 6.71 0.00016 0.00037 0.00178 0.00005 0.00030 0.00001 0.00003 0.00037 0.00004 5.47 0.58 8.02 9.86 8.71 6.83 0.00027 0.00014 0.00034 0.00020 0.00046 0.0004035 0.00004 0.00010 0.00007 0.00001 0.00010 0.00014 5.01 7.23 6.74 9.18 7.23 6.17 0.00034 0.00018 0.00050 0.00027 0.00021 0.00057 349 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 a South -100 -50 P b North 0 50 100 150 200 250 South 300 -3 -2 P/B North -1 0 1 2 3 A. agilis B. arctica B. megalops E. neapolitana L. gracilis L. typicus M. parva A. mimonectes B. longirostris B. typica I. ilergetes L. manco N. tumida R. caeca R. grimaldii R. integricauda R. rostrata S. christianensis S. affinis S. pusilla W. rectirostris D. furcatum I. longicornis M. atlanticus C. glabra C. sulcata C. verrucosa D. serrata H. normani P. armata Fig. 6. Differences of secondary production (P, R index) (a) and P/B (b) of target species between the study areas to the south and northwest of Mallorca. Jurado et al., 2008; Millot, 1999), which may have an effect on local food supply (Fernández de Puelles et al., 2004; Cartes et al., 2008b). This explains both the higher food consumption, energy content of diets and fecundity of top predators inhabiting the N area (i.e. Merluccius merluccius: Cartes et al., 2008c; Hidalgo et al., 2008; Aristeus anetnnatus: Cartes et al., 2009a; Guijarro et al., 2008;). The N area is subject to high productivity events (Estrada, 1996; Bosc et al., 2004), induced by the occurrence of stronger frontal systems linked to Northern and Balearic currents ﬂowing along the slope (see Fig. 1 in López-Jurado et al., 2008), which in turn may contribute to increased zooplankton biomass (Cartes et al., 2008b). Frontal systems are especially strong in the Balearic sub-basin during winter, due to the intensity of winter winds (López-Jurado et al., 2008), decreasing in spring. By contrast, the Algerian basin is subject to more unpredictable events such as eddies generated by entry of Atlantic waters through the Straits of Gibraltar (López-Jurado et al., 2008). The occurrence/ persistence of frontal systems at N may also explain: i) the highest diversity being found there at ca. 400 m, and ii) the shape of its P/B vs depth relation, with highest P/B values at ca. 400–500 m (Fig. 7). According to Font (1987) frontal thermohaline systems impinge on the slope in the Balearic Basin at ca. 400 m depth. Differences in the oceanographic regimes of the two areas could further explain the greater inﬂuence of seasonality along the N transect. The N area was inﬂuenced by a stronger “succession” in the temporal arrival of different water masses. The Winter and Levantine Intermediate waters (WIW, LIW mainly distributed between 150–300 m and 350–550 m respectively) arrived at N during April (WIW) and June (LIW), respectively (López-Jurado et al., 2008). WIW is characterized by minimum temperatures, while LIW has the region's maximum values of salinity and temperature for mid-slope waters (ca. over 300– 500 m bottoms). The Western Mediterranean Deep Waters (WMDW), ﬂowing below LIW, may interrupt the constant northward ﬂow of LIW, especially during winter (López-Jurado et al., 2008). In summary, WIW, LIW and WMDW ﬂow seasonally, arriving sequentially at the N transect, making oceanographic conditions more variable throughout the year than at S. The S area, lacking strong oceanographic frontal systems, constitutes a more uniform, stable, environment (LópezJurado et al., 2008). As a consequence no marked seasonal patterns in suprabenthos were found at S, and its faunal variation was mainly related to depth, particularly related to changes of T and S in the nearbottom water column. Both variables are more dependent upon depth at S (Cartes et al., 2008b). 350 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 0,1000 a peaks were evident at N: Cartes et al., 2008b), we hypothesize that the N transect must be more productive of suprabenthos through the inﬂuence of advective inputs of water masses, e.g. the WIW arriving from neighboring, highly productive, areas (e.g. the Gulf of Lyons). 0,0100 P 0,0010 4.1. Depth-related and spatial mesoscale trends in supranbenthos production and diversity 0,0001 0,0000 15 12 9 P/B 6 3 R2 = 0.225 0 0 200 400 600 800 CoG (m) Fig. 7. Distribution of secondary production (P) and P/B of target species vs their centre of gravity (CoG) in the two areas at S (empty dots) and N (black dots) of Mallorca. The possible inﬂuence of primary production on the diversity and productivity of the near-bottom suprabenthic community may consist of a local enrichment of sediments below the oceanographic front over the slope. This is apparent when comparing the available environmental information from our transects north and south of Mallorca: i) There is a substantial increase, ca. 3-fold, in %TOM (total organic matter) in sediments during April–June at N, coinciding with a parallel increase of suprabenthos biomass (Cartes et al., 2008b). Although %TOM does not speciﬁcally indicate fresh input of organic matter and annual average TOM values are only slightly higher at N (4.9%) than at S (4.0%), the spring increase would indicate new OM inputs. ii) REDOX potential is reduced in sediments at N in April–June (ca. −10 mV) compared with values at S, also suggesting a high input of fresh OM (Cartes et al., 2008b). iii) The C/N of suprabenthos species analyzed in both areas indicated higher C/N and thus greater lipid content and better nutrition in the fauna at N (C/N ranging from 4.6 to 5.2 at N compared to 3.5 to 4.5 at S) (data in Fanelli et al. 2009a; Madurell et al. 2008). This may indicate higher C/N ratios in sediments (fresh OM, because C/N is an indirect measure of lipid content), considering the low trophic level (on average) of suprabenthos. This is further consistent with tendencies discussed above for top predators (Merluccius merluccius: Cartes et al., 2008c; Hidalgo et al., 2008; Aristeus anetnnatus: Cartes et al., 2009a; Guijarro et al., 2008). iv) The stable isotope analysis (SIA) results performed at N (Madurell et al. 2008) and S (Fanelli et al. 2009a) suggest greater input of fresh OM at N. Higher δ13C vs δ15N correlations found at N after the peak of surface primary production are evidence for that (Fanelli et al. 2009a). So, there is a general tendency at N for larger stocks and production affecting all the levels of the trophic web from macrofaunal detritus feeders to ﬁsh and large crustaceans. As Chl a in surface waters estimated from satellite imagery showed similar values and temporal tendencies in both areas (only some longer durations of Chl Secondary production showed a depth related trend. At the shelf-slope break were species with low P/B ratios (Fig. 7). Most of those had a univoltine life-cycle, particularly Anchialina agilis with a single peak of abundance in August–September. It was also univoltine on the Bay of Biscay shelf (Sorbe, unp. data), showed a single peak of abundance in December off Ebro Delta at 50–60 m (Cartes et al., 2007) and in winter on the Adriatic Sea shelf (Ligas et al. 2009). Oostegal females were found in August off NW Mallorca and in December in shelf populations close to Ebro Delta (Cartes et al., 2007), so perhaps the unimodal pattern found here was biased by a seasonal offshore/inshore migratory movement or by incomplete sampling of the depth range occupied by shelf-break species. Bimodal patterns in abundance were prevalent among species living deeper on the slope. Around Mallorca we found differences in production comparing the N and S transects, with a decrease of production with depth at S and higher P/B at intermediate depths at N. Cartes et al. (2009c) found shortscale (ca. 5 km) variations in P/B found off the Ebro River (linked to differences in temperature and organic matter (food supply) between stations. The slightly higher T (b0.05 °C) found to the south of Mallorca is not likely to have had a signiﬁcant inﬂuence on either the degree of degradation of fresh POM arriving at the bottom or the P/B values of resident species. So, the higher P/B at intermediate depths at N was more likely due to greater %OM in sediments generated by the inﬂuence of overlying frontal systems. As a consequence, P/B was greater at N among omnivore-detritus feeders (e.g. Andaniexis mimonectes, Lepechinella manco, all cumaceans), coupled to enriched OM in sediments, while at S carnivores on mesoplankton (all Rhachotropis spp.) had the higher P/B (Fig. 6). Suprabenthos have a wide range of feeding strategies, from deposit and ﬁlter-feeders to carnivores, shown by the wide range of δ15N signals (Madurell et al., 2008; Fanelli et al., 2009a), and species can occupy different habitats in relation to the available food. According to the intermediate disturbance ecological hypothesis [adopted to Deep Sea Biology by Gage and Tyler (1991) from trends found in the diversity of trees in tropical rain forests and corals on tropical reefs (Connell, 1978)], the highest diversity is generally achieved in a nonequilibrium state that, if is not disturbed further, will progress toward lowdiversity. A combination of physical (e.g. turbidity, bottom currents…) and biological factors (dispersal capability of species, trophic factors) disturb deep ecosystems controlling their diversity. Thus, diversity patterns vary according to environmental stability. Around Mallorca stability was higher deeper on the slope in terms of water masses present and also greater to the south of the island due to seasonally more uniform hydrographic conditions (López-Jurado et al., 2008). Trophic factors can inﬂuence diversity, growth rates and P/B ratios of the lowest trophic levels. Predation pressure (Dayton and Hessler, 1972) can maintain different levels of biodiversity at distinct, local or regional, spatial scales. Finding the lowest diversity at the shelf break around Mallorca, compared to deeper slopes, might be a consequence of strong hydrodynamism. The increase of diversity with depth of suprabenthos was parallel to an increase of TOM down the slope (Cartes et al., 2008b), which is indicative of higher deposition rates and of a greater environmental stability deeper. This general depth-related pattern was, however, locally broken by the high diversity linked to the highest P/B of species at ca. 400–500 m along the N transect. In conclusion, on the upper slope at N the inﬂuence of frontal systems and the higher ﬂow of different water masses (WIW and LIW) increased natural disturbance in the area, increasing P/B and diversity of suprabenthic peracarids at the BBL. The average 351 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 distribution of species, their mean CoG, was shallower at N compared to S, which is an indicator of more favorable habitat conditions for suprabenthos at N in the range from 400 to 500 m. This could be because P/B increases in populations submitted to some degree of disturbance (e.g. by human activities such as trawling: Jennings et al., 2001). Regarding diversity trends there are few empirical studies relating diversity and production in the deep sea. Diversity among planktonic copepods is higher in oligotrophic regions, and lower in upwelling areas (Rombouts et al., 2009). Benthic taxa exhibit the same general latitudinal gradients as zooplankton at a global scale, though some taxa (i.e. molluscs) can achieve high diversity (hotspots) also at a regional scale (Crame, 2000). This is somewhat similar to the trend found around Mallorca for peracarids at a mesoscale, with diversity at N being linked to hotspots of better productivity (higher disturbance) at intermediate depths. By contrast, in other benthic taxa (e.g. foraminiferans) higher diversity is found in areas with rather low productivity better production, used in a wide sense, decreasing for example in the North Atlantic basin where there is an abundant deposition of food (phytodetritus: Corliss et al., 2009). This suggests that the relationships between diversity and production may depend, further than the scale adopted, on the trophic levels under analysis, in other words on the proximity of target taxa to the primary food sources that they exploit. Acknowledgments The authors thank to all participants in the project IDEA (ref. REN2002-04535-C02-02/MAR) especially to participants on board the F/V Moralti Nou crews (Dr. J. L. López Jurado and Mr. M. Serra from the Centre Oceanogràﬁc de Balears, I.E.O.). We also thank the technical assistance in the sorting of Dr. T. Madurell and V. Papiol (I.C.M. Barcelona) on board and at laboratory. In its ﬁnal stage objectives of this study were designed within and ﬁnanced by the project ANTROMARE (CTM2009-12214-C02-01-MAR). We thank Dr. J. Junoy (Universidad de Alcala de Henares) for his help in the identiﬁcation of Aega incisa. Appendix 1 Depth range and mean abundances of suprabenthos at N (a) and S (b) of Mallorca Taxa Decapoda Aristeus antennatus (Risso, 1816) Funchalia woodwardi Johnson, 1867 Gennadas elegans (Smith, 1882) Hippolyte cf. huntii (Gosse, 1877) Parapenaeus longirostris (Lucas, 1846) Pasiphaea multidentata Esmark, 1866 Philocheras bispinosus (Hailstone, 1835) Philocheras echinulatus (M. Sars, 1861) Plesionika acanthonotus (S. I. Smith, 1882) Plesionika gigliolii (Senna, 1903) Plesionika martia (A. Milne-Edwards, 1883) Polycheles typhlops Heller, 1862 Pontocaris lacazei (Gourret, 1887) Pontophilus norvegicus (Sars, 1861) Pontophilus spinosus (Leach, 1815) Processa nouveli Al-Adhub & Williamson, 1975 Sergestes arcticus Kröyer, 1855 Sergia robusta (Smith, 1882) Euphausiacea Euphausia krohni (Brandt, 1851) Meganyctiphanes norvegica (M. Sars, 1857) Nematoscelis megalops G. O. Sars, 1883 Stylocheiron sp. G.O. Sars, 1883 Thysanopoda aequalis Hansen, 1905 Euphausiacea unid.D Mysidacea Anchialina agilis (G.O. Sars, 1877) Boreomysis arctica Krøyer, 1861 Boreomysis megalops G. O. Sars, 1872 Calyptomma puritani W. Tattersall, 1909 Dactylamblyops sp. Holt and W. M. Tattersall, 1906 Erythrops neapolitana Colosi, 1929 Eucopia hanseni Nouvel, 1942 Haplostylus sp. J Kossmann, 1880 Leptomysis gracilis (G.O. Sars, 1864) Lophogaster typicus M. Sars, 1857 Mysideis parva Zimmer, 1915 Paramblyops rostrata Holt & Tattersall, 1905 Parapseudomma calloplura (Holt & Tattersall, 1905) Parerythrops lobiancoi W. Tattersall, 1909 Pseudomma sp. D G.O. Sars, 1870 Siriella norvegica (G.O. Sars, 1869) Amphipoda Gammaridea Ampelisca dalmatina G. Karaman, 1975 Ampelisca sp. kröyer, 1842 Bathymetric Abundance distribution N S 692 670 666–760 150 335 727 155 161–376 356–749 347–692 356–748 611–692 155–760 682 376 150–692 666–670 749 – – 0.101 0.023 – 0.007 – 0.032 – – – 0.018 0.034 0.009 0.011 0.178 – – 150–753 363–760 156–760 156 611–753 156–727 0.122 0.054 0.541 – 0.015 0.309 134–376 335–760 155–376 363–748 363–727 153–749 675–760 161–670 153–687 155–692 347–752 347–760 134–749 363–749 347–363 161–670 2.633 6.249 9.775 0.017 0.025 0.538 0.059 0.322 0.213 1.113 1.018 0.369 0.106 0.135 – 0.043 155–363 150–363 – 0.030 Taxa Rhachotropis cf. gracilis Bonnier, 1896 Rhachotropis grimaldii (Chevreux, 1888) Rhachotropis integricauda Carausu, 1948 Rhachotropis rostrata Bonnier, 1896 Rhachotropis spp. D Smith, 1883 Scopelocheirus hopei (A. Costa, 1851) Sophrosyne hispana (Chevreux, 1888) Stegocephaloides christianensis (Boeck, 1871) Synchelidium maculatum Stebbing, 1906 Syrrhoe angulipes Ledoyer, 1977 Syrrhoe afﬁnis Chevreux, 1908 Syrrhoe sp. Goes, 1866 Syrrhoidae G.O. Sars,1895. Syrrhoites cf. barnardi Karaman, 1986 Syrrhoites pusilla Enequist, 1949 Tmetonyx similis (G. O. Sars, 1891) Tryphosella cf. longidactyla Ruffo, 1985 Tryphosella sp. Bonnier, 1893 Tryphosites alleni Sexton, 1911 Tryphosites longipes (Bate & Westwood, 1861) 0.285 Urothoe corsica Bellan-Santini, 1965 0.111 Urothoe elegans (Bate, 1856) 0.375 Westwoodilla caecula (Bate, 1857) 0.011 Westwoodilla rectirostris (Della Vale, 1893) 0.018 Amphipoda Hyperiidea 0.011 Anchylomera blossevillei Milne-Edwards, 1830 Hyperia latissima Bovallius, 1887 1.035 Hyperia schizogeneios Stebbing, 1888 9.676 Hyperiidea unid. 10.743 Hyperoche kroyeri Bovall, 1887 0.080 Lycaeidae Claus, 1879 0.385 Phronima sedentaria (Forskal, 1775) 0.935 Phrosina semilunata Risso, 1822 0.009 Primno macropa Guérin-Méneville, 1836 0.042 Pseudolycaea pachypoda (Claus, 1887) 1.186 Scina borealis (G. O. Sars, 1895) 0.688 Scina crassicornis (Fabricius, 1775) 0.590 Vibilia armata Bovallius, 1887 1.377 Vibilia cultripes Vosseler, 1901 0.345 Amphipoda Caprellidea 0.973 Parvipalpus major Carausu, 1941 0.051 Isopoda 0.270 Aega incisa Schioedte and Meinert, 1879 Anthuridae Leach, 1814 0.100 Belonectes parvus (Bonnier, 1896) 0.120 Natatolana borealis (Lilljeborg 1851) 0.009 0.012 0.131 – 0.007 – 0.062 0.018 0.050 0.267 0.053 0.009 0.098 – – 0.177 0.054 0.009 Bathymetric Abundance distribution N S 696 153–760 155–747 335–752 356–692 150–749 155 156–749 347–747 363 347–752 752 365 363–365 328–752 347–682 695 670 134–752 153–752 347–752 749 352–611 148–747 – 3.495 0.596 1.533 0.028 1.010 – 1.092 0.669 – 0.866 – 0.011 0.021 0.560 0.008 0.031 – 0.745 0.106 0.372 – – 0.630 0.035 1.434 3.215 1.756 0.011 1.018 0.009 0.691 0.128 0.011 1.684 0.020 – 0.054 0.737 0.009 – 0.012 0.418 1.728 0.158 0.009 0.031 1.047 670 370–734 134–760 155–695 148–753 150 150–729 148–760 150–734 171–675 670–769 148–760 356–753 747 0.020 0.060 0.138 0.008 0.009 0.012 0.086 0.068 0.106 0.010 0.007 0.039 0.101 – – – 0.075 0.009 0.062 – 0.009 0.019 0.007 0.011 0.065 0.029 0.158 0.010 161–363 0.036 0.018 148–752 365–749 156–749 134–748 – 0.056 0.297 0.109 0.087 0.018 1.514 0.239 (continued on next page) 352 J.E. Cartes et al. / Journal of Sea Research 65 (2011) 340–354 Appendix 1 (continued) (continued) Taxa Amphilochoides serratipes (Norman, 1869) Amphilochus brunneus Della Valle, 1893 Andaniexis mimonectes Ruffo, 1975 Aoridae Poche, 1908 Arculﬁa trago mediterranea G. Karaman, 1986 Arrhis mediterraneus (Ledoyer, 1983) Atylus sp. Leach, 1815 Bathymedon acutifrons Bonnier, 1896 Bathymedon banyulsensis Ledoyer, 1983 Bathymedon longirostris Jaume, Cartes and Sorbe, 1998 Bathymedon monoculodiformis Ledoyer, 1983 Bathymedon sp.D Sars, 1892 Bruzelia typica Boeck, 1871 Corophium spp. Latreille, 1806 Epimeria parasitica G. O. Sars, 1858 Eusirus leptocarpus G. O. Sars, 1895 Eusirus longipes Boeck, 1861 Gammaridae Latreille, 1802 Gammaridea unid. D Halice abyssi Boeck, 1871 Halice walkeri (Ledoyer, 1973) Halicreion aequicornis (Norman, 1869) Haploops nirae Kaim-Malka 1976 Harpinia cf. crenulata (Boeck, 1871) Harpinia truncata G. O. Sars, 1891 Harpinia spp. Boeck, 1876 Idunella pirata Krapp-Schickel, 1975 Ileraustroe ilergetes (J. L. Barnard, 1964) Lembos sp.J Bate, 1857 Lepechinella manco J.L. Barnard, 1973 Lepidepecreum subclypeatum Ruffo & Schiecke, 1977 Leucothoe lilljeborgii Boeck, 1861 Lysianassa plumosa Boeck, 1871 Lysianassidae J (LeCroy, 2007) Maera schmidti Stephensen, 1915 Megamphopus sp. Norman, 1869 Melitidae Bousﬁeld, 1977 Melphidippella macra Norman, 1869 Metaphoxus simplex (Bate, 1857) Monoculodes packardi Boeck, 1871 Monoculodes acutipes Ledoyer, 1983 Monoculodes griseus (Della Valle, 1893) Monoculodes sp. D Stimpson, 1853 Nicippe tumida Bruzelius, 1859 Normanion ruffoi Diviacco & Vader, 1988 Oediceroides pilosa Ledoyer, 1983 Oediceropsis brevicornis Lilljeborg, 1865 Oedicerotidae Lilljeborg, 1865 Orchomene humilis (A. Costa, 1853) Orchomene grimaldii Chevreux, 1890 Orchomenella nana (Kroyer, 1846) Paracentromedon crenulatum (Chevreux, 1900) Paraphoxus oculatus (G. O. Sars, 1879) Pardalisca mediterranea Bellan-Santini, 1985 Pardaliscidae Boeck, 1871 Perioculodes longimanus (Bate and Westwood, 1868) Phoxocephalidae sp. 1 G.O. Sars, 1891 Pleusymtes sp. J. L. Barnard, 1969 Podoprion bolivari Chevreux, 1891 Pseudotiron bouvieri Chevreux, 1895 Rhachotopis caeca Ledoyer, 1977 Rhachotopis glabra G. O. Sars, 1878 Bathymetric Abundance distribution N S Taxa Bathymetric Abundance distribution N S 362–373 155–747 150–752 376–670 363–670 328–749 161 362–749 356–752 335–760 356–749 692 156–760 363–749 134–752 365–752 347–749 153 134–155 363–749 370–748 363–747 134 365 376 155–747 365–747 335–752 363–365 328–749 347–752 155–749 670–752 155–749 650–696 150–365 189 150–376 356–749 155–749 352–749 161–189 155–747 335–752 363 363–749 328–760 152–747 363–696 376–734 328–752 696 370–734 611–752 363 153–670 347 155 732–747 335–752 134–760 666–692 Natatolana cf. borealis Cymothoidae Leach, 1814 Chelator chelatus Stephensen, 1915 Desmosoma lineare (G. O. Sars, 1899) Disconectes cf. phallangium (G. O. Sars, 1864) Disconectes furcatum (GO Sars, 1870) Disconectes spp Wilson & Hessler, 1981 Eugerda ﬁlipes (Hult, 1936) Eurycope sp. G. O. Sars, 1864 Eurycopidae sp. 1 Hansen, 1916 Eurydice cf. grimaldii Dollfus, 1888 Gnathia maxillaris (Montagu, 1804) Gnathia sp.L Leach, 1814 Ilyarachna longicornis (G. O. Sars, 1864) Ischnomesus bispinosum G.O. Sars, 1865 Munnopsis beddardi (Tattersall, 1905) Munnopsurus atlanticus (Bonnier, 1896) Syscenus infelix Harger, 1880 Isopoda unid. D Cumacea Bathycuma brevirostris (Norman, 1879) Bodotria scorpioides (Montagu, 1804) Campylaspis cf. Macrophthalma G. O. Sars, 1879 Campylaspis glabra G. O. Sars, 1878 Campylaspis horridoides Stephensen, 1915 Campylaspis rostrata Calman, 1905 Campylaspis sp. G. O. Sars, 1865 Campylaspis squamifera Fage, 1929 Campylaspis sulcata G. O. Sars, 1870 Campylaspis vitrea Calman, 1906 Camylaspis verrucosa G. O. Sars, 1866 Cumella spinoculata G.O. Sars, 1865 Cumellopsis puritani Calman, 1905 Cyclaspis longicaudata G. O. Sars, 1865 Diastylis doryphora Fage, 1940 Diastylis tumida (Liljeborg, 1855) Diastyloides bacescoi Fage, 1940 Diasylis sp. Say, 1818 Diatyloides serrata (G. O. Sars, 1865) Diastylidae Bate, 1856 Epileucon ensis Bishop, 1981 Eudorella truncatula (Bate, 1856) Hemilamprops normani Bonnier, 1896 Leptostylis macrura G. O. Sars, 1870 Leptostylis sp.D G. O. Sars, 1869 Leucon afﬁnis (Fage, 1951) Leucon longirostris (Caiman, 1906) Leucon siphonatus (Calman, 1906) Makrokylindrus anomalus (Bonnier, 1896) Makrokylindrus gibraltarensis (Bacescu, 1961) Makrokylindrus insignis (G. O. Sars, 1871) Makrokylindrus longipes (G. O. Sars, 1871) Makrokylindrus stebbingi Stephensen, 1915 Makrokylindrus sp. Stebbing, 1912 Nannastacidae (Cumella sp.) Nannastacus unguiculatus (Bate, 1859) Platysympus typicus (G. O. Sars, 1869) Procampylaspis armata Bonnier, 1896 Procampylaspis bonnieri Calman, 1906 Procampylaspis mediterranea Ledoyer, 1987 Procampylaspis sp. Bonnier, 1896 Vemakylindrus hastatus (Hansen, 1920) 650–752 161–696 347–760 376–749 365–747 150–749 156–749 365–760 365 153–749 155–749 161 134–760 153–752 376–747 150–682 150–760 362–370 696–749 – 747–749 134–370 347–747 150–752 362–749 692 153–670 682 148–752 670–749 171–752 365–747 347–376 171–752 749 328–734 362–376 362 156–752 356–363 376–692 365 328–734 150–749 747 171–752 161–752 363–734 153 171–752 156–376 148–376 347–670 376 363 150–692 171–752 153–760 347–747 376 347–747 365–376 0.080 0.024 2.393 0.011 – 1.038 – 0.199 0.111 0.821 0.036 – 1.413 – 0.063 0.048 0.166 – 0.023 0.084 0.052 – 0.023 0.011 0.033 0.060 0.054 0.966 0.019 1.808 0.325 0.038 – 0.008 – 0.022 0.035 0.023 0.033 0.355 0.169 0.012 0.051 0.772 – 0.011 0.164 0.042 0.075 0.051 1.125 – 0.095 0.094 – 0.011 – – 0.029 0.548 2.416 – 0.065 0.195 1.942 0.012 0.045 0.302 0.009 0.145 0.167 1.912 0.167 0.009 1.476 0.084 0.440 0.160 0.133 0.011 0.018 0.092 0.097 0.041 – – – 0.158 0.010 1.132 – 1.088 0.704 0.075 0.070 0.073 0.015 – – 0.028 0.069 0.363 0.321 0.009 0.052 1.049 0.022 0.059 0.188 0.072 0.021 0.056 0.702 0.007 0.007 0.108 0.011 0.176 0.009 0.009 0.011 0.338 4.301 0.016 References Anderson, M.J., Legendre, P., 1999. 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