Populations of the same species can experience different responses to the environment throughout their distributional range as a result of spatial and temporal heterogeneity in habitat conditions. This highlights the importance of understanding the processes governing species distribution at local scales. However, research on species distribution often averages environmental covariates across large geographic areas, missing variability in population-environment interactions within geographically distinct regions. We used spatially explicit models to identify interactions between species and environmental, including chlorophyll a (Chla) and sea surface temperature (SST), and trophic (prey density) conditions, along with processes governing the distribution of two cephalopods with contrasting life-histories (octopus and squid) across the western Mediterranean Sea. This approach is relevant for cephalopods, since their population dynamics are especially sensitive to variations in habitat conditions and rarely stable in abundance and location. The regional distributions of the two cephalopod species matched two different trophic pathways present in the western Mediterranean Sea, associated with the Gulf of Lion upwelling and the Ebro river discharges respectively. The effects of the studied environmental and trophic conditions were spatially variant in both species, with usually stronger effects along their distributional boundaries. We identify areas where prey availability limited the abundance of cephalopod populations as well as contrasting effects of temperature in the warmest regions. Despite distributional patterns matching productive areas, a general negative effect of Chla on cephalopod densities suggests that competition pressure is common in the study area. Additionally, results highlight the importance of trophic interactions, beyond other common environmental factors, in shaping the distribution of cephalopod populations. Our study presents a valuable approach for understanding the spatially variant ecology of cephalopod populations, which is important for fisheries and ecosystem management.
Citation: Puerta P, Hunsicker ME, Quetglas A, Álvarez-Berastegui D, Esteban A, González M, et al. (2015) Spatially Explicit Modeling Reveals Cephalopod Distributions Match Contrasting Trophic Pathways in the Western Mediterranean Sea. PLoS ONE 10(7): e0133439. https://doi.org/10.1371/journal.pone.0133439
Editor: Brian R. MacKenzie, Technical University of Denmark, DENMARK
Received: February 19, 2015; Accepted: June 26, 2015; Published: July 22, 2015
Copyright: © 2015 Puerta et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Data Availability: Information about surveys and data collected are available at the Data Collection Framework (European Union) website (http://datacollection.jrc.ec.europa.eu/). Raw data was collected by, and stored in, the Spanish Institute of Oceanography (IEO) databases. The dataset is owned by the EU and the IEO and is available upon request to those institutions. For further information and data ordering, contact Enric Massutí (firstname.lastname@example.org), the coordinator of MEDITS surveys in the study area.
Funding: This research is supported by the project "ECLIPSAME" (Synergistics effects of Climate and Fishing on the demersal ecosystems of the North Atlantic and western Mediterranean, CTM2012-37701) co-financed by the Spanish Ministry of Economy and Competitiveness (http://www.mineco.gob.es/) and the European Commission. Surveys were co-funded by the Directorate-General for Maritime Affairs and Fisheries (DG-MARE) of the European Commission (http://ec.europa.eu/dgs/maritimeaffairs_fisheries/index_en.htm) and the Spanish Institute of Oceanography (www.ieo.es). PP is supported by the funding of FPI grant BES-2010-030315 from the Spanish Ministry of Economy and Competitiveness. MEH’s funding is provided by the Gordon and Betty Moore Foundation, grant number 2897.01, (www.moore.org) through the “Ocean Tipping Points” project (www.oceantippingpoints.org). MH is supported by the European Community's Seventh Framework Programme (FP7/2007–2013) under grant agreement MYFISH n° 289257 (www.myfishproject.eu/) and a postdoctoral contract of the Dirección General d'Educació, Personal Docent, Universitats i Recerca (http://dguni.caib.es/) funded by the European Social Fund 2014–2020 (http://ec.europa.eu/esf/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Interaction between species distribution and the environment is a central topic in ecology. Not all species or populations are able to inhabit areas with their most favourable conditions due to the presence of competitors, limited resource availability, anthropogenic impacts and other drivers that may prevent their establishment in certain areas. Therefore, populations of the same species can experience different responses to the environment throughout their distributional range, as a result of spatial and temporal heterogeneity in habitat conditions.
In species distribution models, environmental covariates (e.g. sea surface temperature, SST, in marine species) are often averaged across large geographic areas. By applying average conditions homogeneously over space, important local effects on populations and nonlinear species–environment interactions may not be detected [1,2], and important ecological mechanisms that regulate population abundance and distribution at small scales might remain unknown. However, a deeper understanding of local scale processes governing species distribution and their habitat selection is important for identifying essential areas for survival, reproduction or feeding .
Spatially variant or spatially explicit models have become of particular interest in the recent years [3–6], because they can improve our understanding of the interactions between population distributions and environmental influences within geographically distinct habitats or areas. For instance, variable coefficient Generalized Additive Models (vc GAM) have been successfully applied to describe the locally variant effects of temperature on the distribution of several groundfishes [2,7,8] and albacore tuna  in the northeast Pacific Ocean.
Despite the utility of spatially explicit models for studying heterogeneity in population abundance, especially in species with highly variable dynamics, they have been applied very rarely to marine taxa other than fish [9,10]. Yet, this modelling approach can be useful for studying cephalopod populations, which are highly sensitive to environmental conditions owing to their short life-cycles and reduced demographic buffering . Like other short-lived species with intrinsically unsteady dynamics, cephalopod populations are rarely regular in abundance and location, displaying different adaptations to local environmental conditions throughout their geographic distribution. For instance, there is high variation in the abundance, biological parameters and life-cycle of Loligo vulgaris across the Atlantic Ocean and the Mediterranean Sea, which are attributed to adaptation of populations to large-scale environmental variability . Similar results were recently found for the cephalopods Illex coindetii, Eledone cirrhosa and Octopus vulgaris in the western Mediterranean Sea. The seasonal cycles and the inter-annual distributions differ with geographical location in response to contrasting regional environmental drivers, irrespectively of species-specific life history traits [13,14]. The different adaptations of the cephalopod populations in the Mediterranean Sea are related to the high complexity of this system, which presents diverse hydrodynamic areas [15,16] and different productivity regimes [17,18] at relatively small spatial scales.
In addition to the environmental influence, trophic relationships are one of the main mechanisms that locally affect spatio-temporal abundance and distribution of marine populations. For instance, prey-predator spatio-temporal overlap and prey availability are essential for the survival of predators, as proposed by the match-mismatch hypothesis [19,20]. In turn, these trophic interactions can also be directly or indirectly modified by the environmental forcing. Trophic relationships have been suggested to be no less important than the environment in shaping cephalopod populations . However, the inclusion of predator–prey interactions in cephalopod population models is still rare.
Because recent studies show that temporal variability in the cephalopod populations presents different drivers and responses in neighbouring geographic regions, we hypothesize that spatial variability in the distributions of these species may be sensitive to local variation of drivers influencing the distribution. In this case, the cephalopod populations may present spatially variant effects associated with the variability in environmental and trophic conditions at local scales. Here we aim to develop a spatially explicit modelling approach to (1) identify the spatial variability in the regional distribution of two of the most abundant cephalopods in the western Mediterranean Sea, the squid Illex coindetii and the octopus Eledone cirrhosa (henceforth referred to as squid and octopus, respectively). (2) In addition to environmental explanatory variables, we test the importance of trophic conditions, i.e. prey densities, as a driver of the variability in spatial distribution patterns. (3) The approach specially focuses in detecting areas where the populations are more sensitive to a given explanatory variable within their distributional range, i.e. spatial local effects.
Materials and Methods
Biological data were obtained from the annual trawl surveys carried out as part of the Mediterranean International Trawl Survey (MEDITS) project. The sampling was performed under repeated international standardized protocol (details of the survey methods can be found in ). The surveys were mainly conducted across the Spanish territorial waters in the Mediterranean Sea. The research vessel had full permission from national (Fisheries General Secretariat) and international authorities (General Fisheries Commission for the Mediterranean) to sample in territorial and Mediterranean community waters. No approval by an ethics committee was required as common exploited species were targeted and trawling did not affect endangered or protected species or marine protected areas. Most of the authors participate consistently in the surveys of the MEDITS programme.
The MEDITS surveys took place between May and July in years 2001 to 2012 in the Spanish western Mediterranean Sea. A similar number of stations were sampled each year (150 annual hauls on average), predefined based on different bathymetric strata (10–50 m, 50–100 m, 100–200 m, 200–500 m and 500–800 m) with approximately replicated locations (Fig 1). An experimental trawl net (GOC 73) was designed for the scientific purposes of the surveys. The gear was tested for the catchability of common benthic and pelagic species at the beginning of MEDITS programme that lead to implement some technical improvements (Bertrand et al 2002). The cod-end is 20 mm mesh size, with ca. 17 and 2.8 m of horizontal and vertical openings, respectively. These characteristics ensure higher catchability of demersal species than those obtained by gears use in commercial fisheries. Sampling information (date, time, position, depth, duration, distance trawled, vertical and wing opening of the net) and species biological data (weight, number, sex and length) were routinely recorded. We restricted our analysis to those stations that were sampled during at least 5 out of the 12 years. Species abundances were standardized using sampling information to obtain density values in individuals per km2. Cephalopod prey densities were also estimated (in individuals per km2) as a potential driver influencing the spatial distributions of the two cephalopod species. Based on stomach content analyses (see methodology in ) of 134 octopus and 265 squid (S1 Table), we identified broad prey groupings for the two species. In addition, species of similar size, depth and habitat distribution as those identified in stomach contents and those encompassed in high taxonomic levels of identification (e.g. species in family Paguridae) were included as potential prey items (S2 Table). In general terms, the diet of octopus consists of benthic crustaceans, mainly crabs, while squid mostly prey on myctophids and other small meso-pelagic fishes. Total densities of cephalopod prey were calculated as the summed densities of all potential prey species occurring at each sampling location (Fig 2A and 2B).
Map of the western Mediterranean Sea showing 200 to 1000 m isobaths and selected stations sampled for at least 5 out of the 12 years in the MEDITS surveys. Main surface circulation patterns are described by arrows: Northern Current (NC), Balearic Current (BC), Atlantic jet (AJ) and Alboran gyres (AG).
A) log transformed density of benthic crustaceans (preys of octopus), B) log transformed density of meso-pelagic fish (preys of squid), C) Chlorophyll a concentration (Chla), and D) sea surface temperature (SST) estimated from variable coefficient Generalized Additive Models.
Other putative environmental drivers, i.e. surface Chla (mg m-3) and SST (°C) derived from satellite remote sensing, were also included in our analysis. Remotely sensed data were obtained from NOAA’s CoastWatch Program (available: http://coastwatch.noaa.gov/. Accessed 03 June 2014) and NASA's Goddard Space Flight Center (available: http://www.nasa.gov/centers/goddard/. Accessed 05 June 2014) using different sensors to match the time range of the sampled data. Chla datasets were obtained from Sea WiFS (2001 to 2002) and MODIS sensors (available since 2003) and processed with standard color algorithms . Whereas AVHRR (2001–2002) [25,26] and MODIS (2003–2012)  supplied SST datasets. Differences in measurements between sensors are relatively minor [28,29], displaying no important impact on the results. Values of Chla and SST in a 9 km radius around each sampled location were extracted from 8-day composites and 4 km resolution files. From these values, monthly averages (previous to the date of sampling) of Chla and SST were calculated at each sampled location (Fig 2C and 2D). The chosen spatial and temporal resolution is appropriate for identifying the local productivity regimes and surface oceanographic processes in the study area, while minimizing cloud impact on the measurements.
Due to the high proportion of zeros in the observations of both species (~50%), we used Delta Generalized Additive Models (GAM) [30,31] to estimate cephalopod distributions. The Delta-GAM includes two different sub-models [32,33]. First, presence-absence data are modelled using a binomial logit GAM (stage 1, Pij) and second, only positive density values are used in a Gaussian GAM with a log link function (stage 2, Dij). Finally, to reduce bias of the sub-models and obtain the overall predictions of Delta-GAM (Yij) the results of both model fits are multiplied (Yij = Pij * Dij). For model selection (see below), the same set of covariates was initially included in stages 1 and 2 of the Delta-GAM for simplicity.
Starting from the Delta-GAM, we developed and contrasted two different model formulations: a full Delta-GAM and a variable coefficient Delta-GAM (vc Delta-GAM). The full Delta-GAM assumes that changes in distribution are homogeneous over space and time, and the effects of covariates are independent and additive. Variable coefficient Delta-GAM, by contrast, tests the spatially variant effects of environmental and trophic drivers on cephalopod distributions. This last formulation assumes that the relationship between response (occurrence or density of a species) and covariates is locally linear, but the coefficients of regression are allowed to change smoothly in relation to the geographical position. The formulation of the two approaches (including stages 1 and 2 in both Delta-GAM) is as follows:
A) A full Delta-GAM of the form: where C is either the probability of cephalopods occurrence (stage 1, Pij) or an estimate of natural logarithm of density when the cephalopods are present (stage 2, Dij). Smoothing functions are denoted by s; ay is the year (y)-specific intercept, geographical position was described by latitude (ϕ) and longitude (λ), DOY indicates the day of the year, prey denotes the natural logarithm of prey densities and Chla and SST are expressed in monthly mean values.
B) A variable coefficient Delta-GAM of the form: in which environmental and trophic covariates (Chla, SST and preys) are tested for potential spatially explicit effects on cephalopod occurrence and density, while the rest of the covariates remained as common smooth terms. To describe the potential spatially explicit effects on cephalopod densities, local coefficients of regression (slopes) of these terms were extracted from the sub-model performed on positive abundance data (stage 2). The values of significant slopes (based on 95% confidence interval) reflect the strength of the effect of a given covariate in cephalopod densities at each geographical position.
All possible combinations of the covariates described above were tested in the model selection. This selection process was applied independently for each stage (occurrence and density) and model formulation (full Delta-GAM and vc Delta-GAM). Independent model structures were used since drivers affecting the presence of a given species are not necessarily the same that influence its abundance [32,34–36]. An independent model selection approach for presence-absence and abundance information is able to address those different drivers and provide better fit of each type of data set. To compare full and reduced versions of the models, we used the Akaike Information Criterion (AIC) as a measurement of goodness of fit, and the genuine Cross Validation (gCV)  as a measure of the out-of-sample predicted mean squared error. The lowest values of both criterions determined the model that best explained the variance of the response and was optimal for predictions. All analyses were conducted using mgcv and MuMIn packages in R software, version 3.1.1 .
Spatial modelling approach
For both cephalopods, the vc Delta-GAM performed better than the full Delta-GAM formulations in terms of AIC, gCV and deviance explained (Table 1). Differences in model fit between the two formulations were relatively minor for octopus, but vc Delta-GAM notably improved the model fit for squid. The best fit in presence-absence vc GAM for octopus explained 37.4% of the deviance, which included, in addition to the base parameters of the models (year, position and depth), the density of prey items and Chla concentration as significant predictors (Table 1). Similarly, day of the year, density of prey items, Chla and SST were included in the presence-absence best sub-model for squid, which explained 33.1% of deviance in its occurrence (Table 1). The density sub-model of the vc GAM explained 32.5% and 43% of the deviance for octopus and squid, respectively. The three spatially variant terms, (prey density, Chla and SST) were retained in density sub-models that best fit the density distributions of the two species (Table 1).
Comparisons of full Delta-GAM and variable-coefficient, vc, Delta-GAM (formulations were simplified). Base term includes Cy,(ϕ,λ) = ay + s1(ϕ,λ) + s2(depth); where Cy,(ϕ,λ) is either the probability of cephalopods occurrence (stage 1, presence-absence sub-model) or an estimate of natural logarithm of density when the cephalopods are present (stage 2, density sub-model); a is the year (y) -specific intercept, latitude ϕ, longitude λ and depth. Other parameters included as smoothing functions (s1-6) in the models are prey, as the natural logarithm of prey densities, day of the year, DOY, monthly average chlorophyll a concentration, Chla and sea surface temperature, SST. For each model and stage AIC: Akaike Information Criterion, AIC: increment of AIC: ΔAIC, gCV: genuine Cross Validation and dev. exp: percentage of deviance explained by the model are given. Best models obtained for each formulation and stages are in bold.
Spatial distribution of cephalopod species
The distributions predicted by the best models confirmed different spatial patterns between octopus and squid (Fig 3). We found high probabilities of occurrence of both species across most of the study area. Low occurrences of both cephalopods were only found in the southern region (Alboran Sea). In contrast, the areas with the highest densities (considering both stages of the best vc Delta-GAM) differed considerably between the two species. The highest densities of octopus were located in the northern region, continuing throughout the offshore waters of southern Ebro river delta and the west shelf of the Balearic Archipelago (Fig 3A). In the case of squid, areas with the highest densities were more limited to the central region, southwards Ebro river delta (Fig 3A). Density values of squid decreased with distance from the central region and high-density areas exhibited less variability in environmental conditions than those occupied by octopus. For both species, the lowest densities were predicted in the southern region, which is mainly characterized by very high Chla concentrations (Fig 2C). Depth had a positive effect on both the occurrence and densities of the two cephalopods. Maximum densities were found between 200–250 m depth, while negative effects were observed at depths lower than 50 m and higher than 400 m (Fig 3B).
Spatially explicit effects of environmental and trophic covariates
We observed significant spatially explicit effects of prey density, Chla and SST on the local density of both cephalopod species (Fig 4). For octopus, the slopes for prey density showed a weak but positive effect in the central region and around the islands (Fig 4A), where intermediate to low prey densities were found (Fig 2A). A notable negative effect of Chla on population density was observed in the southern region (Fig 4B), where the highest values of Chla were recorded (Fig 2C). In contrast, SST showed a localized positive effect on octopus densities only observed in the southern locations of the Balearic Archipelago (Fig 4C).
Effects of A) prey densities, B) chlorophyll a concentration (Chla) and C) sea surface temperature (SST) estimated from variable coefficient Generalized Additive Models using only positive data. Red and blue bubbles represent respectively negative and positive effect of each covariate on log-transformed cephalopod densities. Only effects (regression slopes) significantly different from zero are showed, based on the estimates of the 95% confidence interval. Overall predicted densities (log transformed) of each species are shown underlayed, with the highest densities indicated by dark grey cells.
Very different spatially explicit effects were observed for squid. A positive influence of prey densities on squid was found in the southern region and around the Balearic archipelago (Fig 4A). These effects were much higher in the islands, especially in the western part. Additionally, important negative effects of prey density were detected in the central region surrounding the Ebro river delta. Chla revealed a general and high negative effect for squid densities in the whole study area (Fig 4B). Considerable effects of SST were also found for this species, with local negative slopes in the western part of the archipelago and in the central region, displaying an evident north-south gradient in the strength of the effect (Fig 4C). These regions recorded the highest temperature values of the study area (Fig 2D).
Spatial modelling approach
The spatially explicit modelling approach developed in the present study allowed us to examine the heterogeneity in the spatial abundances of the squid Illex coindetii and the octopus Eledone cirrhosa populations in the western Mediterranean Sea. Our results revealed important local species–environment interactions that drive the abundance and distributional patterns in this geographically and oceanographically complex system. The inclusion of delta models in the approach showed that ecological processes governing presence-absence and densities are partially independent for octopus, but this is not necessarily a general pattern, as we observed in squid. The best model obtained for octopus included different covariates in each of the model stages. While the occurrence was determined by the presence of productive areas (prey densities and Chla), densities were also influenced and SST, which usually dictate recruitment peaks in the seasonal cycle of this species . In contrast, prey densities, Chla and SST were included in both stages for squid, with the day of the year only retained in the presence-absence sub-model, suggesting that similar processes determine both the occurrence and abundance of this species.
Spatial distribution of cephalopod species
One of the most novel results of our study is the contrasting regional distribution pattern obtained for each cephalopod species, observed by combining information from the Balearic Archipelago and the mainland. These contrasting patterns elucidate a species-specific adaptation to the main trophic pathways derived from the bottom-up forcing of primary production regimes observed in the western Mediterranean: the southwards flow of high productive waters originated in the north-western upwelling (the Gulf of Lion) in the case of the octopus and the bottom-up processes triggered by the Ebro river discharges in the case of the squid. The highest occurrence and densities of octopus were located in the northern region and continue towards south-west across the offshore waters and the western shelf of the Balearic Archipelago. This distribution follows the Mediterranean Northern Current pattern (Fig 1), which spreads highly productive waters from the phytoplankton bloom produced by the autumn-winter upwelling from the Gulf of Lions . This makes this area one of the most productive regions in the western Mediterranean Sea, even though it was characterized by low chlorophyll concentrations in spring (as observed in data). A time-lagged response to the upwelling and the dispersion of highly productive waters clearly explains the octopus distribution we found in spring months. This is in accordance with previous research reporting delayed responses of several months to surface environmental conditions (e.g. Chla) in octopus populations from the western Mediterranean [13,40,41].
By contrast, the highest densities of squid were located beneath the Ebro river mouth, in the area influenced by the river plume. Ebro run-off is highest during spring [42,43], but ephemeral discharges depend on wind and rainfall conditions, which can generate intermittent bottom-up production processes. In spring, the solar heating and the decrease in wind activity create a thermocline that inhibits vertical mixing and a depletion of surface nutrients. Therefore, the only source that may contribute to surface primary production, enhancing the trophic cascade, is nutrient inputs from river discharges . Contrary to the benthic octopus, the nektobenthic squid responds to co-occurring conditions due to its stronger association with the water column . Therefore, food availability in the river plume can favour squid recruitment, as have been previously observed in cephalopod populations [40,44,45], including squid . This does not precludes that at local scale, octopus might also be partly influenced by the river discharges [13,40,41].
The southern region (Alboran Sea) presented very low occurrences and densities of both cephalopod species. This region is characterized by a turbulent mixing due to exchanges of Mediterranean and Atlantic waters and persistent anticyclonic gyres (Fig 1) that create highly oligotrophic conditions. However, the incoming Atlantic jet strongly enhances primary and secondary production in surface waters around the gyres , resulting in very high Chla levels in comparison to the other study regions. The instability in primary production and hydrographic conditions might make this area less suitable to cephalopod populations. A non-exclusive explanation might be related to differences in seasonal dynamics of cephalopod populations in the western Mediterranean . Populations from the southern region might display a different seasonal cycle to cope with such unsteady conditions, as suggests the fact that the lowest densities of Octopus vulgaris in this area were observed during spring .
Spatially explicit effects of environmental and trophic covariates
As we hypothesized, spatially explicit effects associated with the variability of environmental and trophic drivers were found in the two cephalopod species across the study area. Prey densities describe the direct link of potential food availability for adult individuals, while Chla is a proxy of productivity and energy flow in the trophic pathway that ultimately influences the yield of upper trophic levels (indirect link). By contrast, there are multiple mechanistic linkages between SST and population distributions, which effects can be interpreted from the physiological to population perspective [11,48,49]. Since the highest densities of the two cephalopods were found between 100–400 m depth, where temperature remains constant during spring (around 13°C ), physiological processes should not influence the observed patterns . Temperature is also directly or indirectly associated with the availability of food resources and consumption rates in marine food-webs , as has been observed in most organisms including cephalopods [51–53].
Prey availability usually constitutes the foremost condition for habitat selection or aggregative response of predators [54,55]. Our results showed, however, that this seems to apply to the distribution of octopus but not to that of squid. Food limited areas can be inferred from spatially explicit effects of prey observed in the two cephalopods. Scarce prey availability was observed for octopus in the Balearic Archipelago and the central region of the mainland, as reflected in the small positive effects of prey abundances. This agrees with distributional maps in those areas, where high densities of octopus matched intermediate prey densities. By contrast, food availability strongly limited squid densities around the archipelago, in accordance with the observed low abundances of both prey and predator. The strength of this effect showed a west-east gradient in the archipelago, suggesting a stronger influence towards the edge of the distribution area of the squid. In another sub-optimal distribution area, such as the Alboran Sea, weak positive effects of prey densities were also observed for squid. Despite the high prey availability recorded in this region, very low densities of squid were found, which might reflect unsteady trophic interactions between prey and predator or the influence of other factors in this highly dynamic oceanographic area. Besides positive local effects of prey density, the spatially explicit approach also allowed identifying the opposite situation for squid in the central region of the mainland around the Ebro river plume. As previously mentioned, river discharges make this area very productive locally, especially for the pelagic system [43,56]. We suggest that the local decrease in squid abundance when high prey densities occur are due to the increase of pelagic competitors and predators because of the high primary production in this region [57,58]. This could explain why we found the high-density distribution of squid in this area, in spite of the lowest prey abundances and the negative effects of prey. It is also worth noting that the small meso-pelagic fish preyed on by squid usually display low catchability with the trawling gear, whereby their abundance values might be biased.
A common pattern was observed in the two species related to Chla, which showed negative effects on cephalopod abundances despite their high-density distributions matching areas of high productivity. Although this might seem counterintuitive, it would be in accordance with the argument of competition pressure described above. The food-web in the western Mediterranean is mainly controlled by small pelagic fishes and changes in their biomass have important consequences for all trophic levels [57,58], especially when food becomes limiting as in oligotrophic seas such as our study area . This seems to be the case for squid, as the negative effect of Chla is widespread in the whole study area. Competition pressure with pelagic fish may indirectly affect inter-annual variability of squid, as primary production enhance fish populations that compete more effectively with the early and juvenile stages of squid, thereby inducing a decrease in their regional density. By contrast, densities of octopus were only negatively influenced by Chla in the Alboran Sea. Although Chla presents more influence in the pelagic than in the benthic system, the high hydrodynamics is also associated with instability in trophic interactions . Therefore, unstable trophic interactions, especially in a sub-optimal area of distribution as this one, could also affect the benthic system and the octopus densities.
Several studies demonstrate that species inhabiting the boundaries of their distributional areas display higher sensitivity to environmental variability . In the present study, SST effects were observed in the distribution limits of both species, where the highest temperatures and oligotrophy levels were recorded. However, opposite effects were found in both species related to SST. Squid populations were negatively affected by temperature. Warmer temperatures create stronger and longer stratified waters by limiting the input of nutrients along with phytoplankton and zooplankton growth. Additionally, inter-annual and seasonal variability in zooplankton abundance show a clear response to warmer periods by reducing biomass and changing the composition and structure of communities . That results in important implications on the productivity and the functioning of the pelagic ecosystem in the western Mediterranean , which can finally limit or reduce the abundance of squid in the warmest areas. The strength of the effect also showed a north-south gradient, probably related to the spreading of north-western highly productive waters. As described above, the northern current spreads colder and productive waters southwards, and forms a branch throughout the northern slope of the Balearic Archipelago (Fig 1). Therefore, the effects of stratification seem to be lower in the north than in the south of the islands. This is in agreement with the contrasting regimes and species responses [62–64], including cephalopods [13,14], observed between both sides of the archipelago. By contrast, octopus showed positive effects of temperature only in the southern Balearic Archipelago. Warmer and more saline waters coming from the Atlantic (AW) are established in this area, having implicitly associated the lowest primary and secondary production in the western Mediterranean. While it is difficult to elucidate how warm temperature benefits octopus densities, we suggest that the most plausible mechanism might be related to the links between surface conditions and benthic environments observed during early summer in the Balearic Islands. When cold western Winter Intermediate Waters (WIW) are present in the channel between islands due to colder winters, northwards progress of the warmer AW throughout the channels is blocked in spring . WIW are also linked to surface AW dynamics and the formation of a mesoscale front in the south of the islands. Inter-annual variation in the presence or absence of the WIW can also modify the temperatures in surface and intermediate waters, and affect the local productivity, planktonic communities [66,67] and meso-pelagic fish  associated with the front. Together with temperature, these mechanisms might directly or indirectly explain the effects observed in octopus densities. However, additional factors not included in our work such as substrate, predation or fishing, cannot be discarded, since they might be also influenced by temperature.
Spatially variant models lead us to better understand cephalopod distributions in heterogeneous and complex systems, such as the western Mediterranean Sea. The spatial heterogeneity in abundance observed in the octopus Eledone cirrhosa and the squid Illex coindetii populations was ascribed to different trophic pathways present in the study area. Contrasting spatially explicit effects were observed in the two species, with stronger effects mostly found in the limits of their distributional range. Additionally, results highlight the importance of trophic interactions, in addition to environmental factors, in shaping cephalopod distributions in a highly oligotrophic system such as the Mediterranean Sea. Local adaptations of cephalopod populations to environmental and trophic conditions were evidenced, suggesting that complex population structures and dynamics are more widespread than expected [13,14,21].
Our study highlights that the knowledge of environmental and trophic effects in the abundance and distribution of cephalopod populations at regional and local scales is needed for marine spatial planning, conservation and management. Additionally, the modelling approach used here can be applied in future investigations of biological responses to climate change, which is expected to induce shifts in marine species distributions and abundances including cephalopods [69–71]. This is paramount in the Mediterranean Sea, where marine populations and food-webs are especially vulnerable to climate change [72–74] and highly dependent on favourable environmental and trophic conditions at small spatial scales [14,57,75].
S1 Table. Diet composition of octopus (Eledone cirrhosa) and squid (Illex coindetii).
Frequency of occurrence (%F) of species identified to the lowest possible taxon in stomach contents.
S2 Table. Main prey species selected for octopus (Eledone cirrhosa) and squid (Illex coindetii).
The frequency of occurence (%F) and cumulative densities (%C.Den) in relation to all potential prey species selected are shown for the 10 main preys found in the MEDITS surveys from 2001 to 2012.
We are very grateful to all scientists and vessel crew that participated in the MEDITS surveys.
Conceived and designed the experiments: PP MEH AQ MH. Performed the experiments: MH AQ AE MG. Analyzed the data: PP MEH MH AQ DAB. Contributed reagents/materials/analysis tools: PP MEH MH AQ DAB AE MG. Wrote the paper: PP MEH MH AQ DAB AE MG. Relevant literature review: PP MEH AQ DAB AE MG MH. Numerical modelling design: PP MEH MH. Software development: PP MEH DAB.
- 1. Bacheler NM, Bailey KM, Ciannelli L, Bartolino V, Chan K- S (2009) Density-dependent, landscape, and climate effects on spawning distribution of walleye pollock Theragra chalcogramma. Mar Ecol Prog Ser 391: 1–12.
- 2. Bacheler NM, Ciannelli L, Bailey KM, Bartolino V (2012) Do walleye pollock exhibit flexibility in where or when they spawn based on variability in water temperature? Deep Sea Res Part II Top Stud Oceanogr 65–70: 208–216.
- 3. Valavanis VD, Pierce GJ, Zuur AF, Palialexis A, Saveliev A, Katara I, et al. (2008) Modelling of essential fish habitat based on remote sensing, spatial analysis and GIS. Hydrobiologia 612: 5–20.
- 4. Andrews JM, Gurney WS, Heath MR, Gallego A, O’Brien CM, Darby C, et al. (2006) Modelling the spatial demography of Atlantic cod (Gadus morhua) on the European continental shelf. Can J Fish Aquat Sci 63: 1027–1048.
- 5. Tyberghein L, Verbruggen H, Pauly K, Troupin C, Mineur F, De Clerck O (2012) Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr 21: 272–281.
- 6. Phillips AJ, Ciannelli L, Brodeur RD, Pearcy WG, Childers J (2014) Spatio-temporal associations of albacore CPUEs in theNortheastern Pacific with regional SST and climate environmental variables. ICES J Mar Sci.
- 7. Bartolino V, Ciannelli L, Bacheler NM, Chan K-S (2011) Ontogenetic and sex-specific differences in density-dependent habitat selection of a marine fish population. Ecology 92: 189–200. pmid:21560689
- 8. Ciannelli L, Bartolino V, Chan K-S (2012) Non-additive and non-stationary properties in the spatial distribution of a large marine fish population. Proc R Soc B Biol Sci 279: 3635–3642.
- 9. Llope M, Chan K-S, Ciannelli L, Reid PC, Stige LC, Stenseth NC (2009) Effects of environmental conditions on the seasonal distribution of phytoplankton biomass in the North Sea. Limnol Oceanogr 54: 512–524.
- 10. Llope M, Licandro P, Chan KS, Stenseth NC (2012) Spatial variability of the plankton trophic interaction in the North Sea: A new feature after the early 1970s. Glob Chang Biol 18: 106–117.
- 11. Pierce GJ, Valavanis VD, Guerra A, Jereb P, Orsi-Relini L, Bellido JM, et al. (2008) A review of cephalopod–environment interactions in European Seas. Hydrobiologia 612: 49–70.
- 12. Moreno A, Pereira J, Arvanitidis C, Robin JP, Koutsoubas D, Perales-Raya C, et al. (2002) Biological variation of Loligo vulgaris (Cephalopoda:Loliginidae) in the eastern Atlantic and Mediterranean. Bull Mar Sci 71: 515–534.
- 13. Puerta P, Hidalgo M, González M, Esteban A, Quetglas A (2014) Role of hydro-climatic and demographic processes on the spatio-temporal distribution of cephalopods in the Western Mediterranean. Mar Ecol Prog Ser 514: 105–118.
- 14. Puerta P, Quetglas A, Hidalgo M (2014) Modelling seasonal variability of cephalopod abundances of three contrasting species from Western Mediterranean Sea. ICES CM 2014/P:02.
- 15. Millot C (1999) Circulation in the Western Mediterranean Sea. J Mar Syst 20: 423–442.
- 16. Millot C (2005) Circulation in the Mediterranean Sea: evidences, debates and unanswered questions. Sci Mar 69: 5–21.
- 17. Bosc E, Bricaud A, Antoine D (2004) Seasonal and interannual variability in algal biomass and primary production in the Mediterranean Sea, as derived from 4 years of SeaWiFS observations. Global Biogeochem Cycles 18: GB1005.
- 18. D’Ortenzio F, Ribera d’Alcalà M (2009) On the trophic regimes of the Mediterranean Sea: a satellite analysis. Biogeosciences 6: 139–148.
- 19. Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the Match/Mismatch hypothesis. Adv Mar Biol 26: 249–293.
- 20. Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33: 271–283.
- 21. Rodhouse PGK, Pierce GJ, Nichols OC, Sauer WHH, Arkhipkin AI, Laptikhovsky VV, et al. (2014) Environmental effects on cephalopod population dynamics: implications for management of fisheries. Adv Mar Biol 67: 99–233. pmid:24880795
- 22. Bertrand JA, Gil de Sola L, Papaconstantinou C, Relini G, Souplet A (2002) The general specifications of the MEDITS surveys. Sci Mar 66: 9–17.
- 23. Valls M, Quetglas A, Ordines F, Moranta J (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Sci Mar 75: 633–639.
- 24. O’Reilly JE, Maritorena S, O’Brien MC, Siegel DA, Toole D, Menzies D, et al. (2000) Ocean color chlorophyll a algorithms for SeaWiFS, OC2, and OC4: Version 4. In: Hooker S. B and Firestone ER, editor. SeaWiFS Postlaunch Technical Report Series. Greenbelt, Maryland: NASA, Goddard Space Flight Center. pp. 9–23.
- 25. Walton CC, Pichel WG, Sapper JF, May DA (1998) The development and operational application of nonlinear algorithms for the measurement of sea surface temperatures with the NOAA polar-orbiting environmental satellites. J Geophys Res Ocean 103: 27999–28012.
- 26. Kilpatrick KA, Podestá GP, Evans R (2001) Overview of the NOAA/NASA advanced very high resolution radiometer Pathfinder algorithm for sea surface temperature and associated matchup database. J Geophys Res Ocean 106: 9179–9197.
- 27. Brown OB, Minnett PJ (1999) MODIS Infrared sea surface temperature algorithm. Algorithm theoretical basis document. Version 2.0. Under Contract Number NAS5-31361. Miami, Florida: University of Miami.
- 28. McCain C, Hooker S (2006) Satellite data for ocean biology, biogeochemistry, and climate research. Eos (Washington DC) 87: 337–343.
- 29. Antoine D, D’Ortenzio F, Hooker SB, Bécu G, Gentili B, Tailliez D, et al. (2008) Assessment of uncertainty in the ocean reflectance determined by three satellite ocean color sensors (MERIS, SeaWiFS and MODIS-A) at an offshore site in the Mediterranean Sea (BOUSSOLE project). J Geophys Res 113: C07013.
- 30. Guisan A, Edwards TC, Hastie T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Modell 157: 89–100.
- 31. Hastie T, Tibshirani R. Generalized additive models. London: Chapman and Hall; 1990.
- 32. Hollowed AB, Barbeaux SJ, Cokelet ED, Farley E, Kotwicki S, Ressler PH, et al. (2012) Effects of climate variations on pelagic ocean habitats and their role in structuring forage fish distributions in the Bering Sea. Deep Sea Res Part II Top Stud Oceanogr 65–70: 230–250.
- 33. Grüss A, Drexler M, Ainsworth CH (2014) Using delta generalized additive models to produce distribution maps for spatially explicit ecosystem models. Fish Res 159: 11–24.
- 34. Koubbi P, Loots C, Cotonnec G, Harlay X, Grioche A, Vaz S, et al. (2006) Spatial patterns and GIS habitat modelling of Solea solea, Pleuronectes flesus and Limanda limanda fish larvae in the eastern English Channel during the spring. Sci Mar 70: 147–157.
- 35. Barry SC, Welsh AH (2002) Generalized additive modelling and zero inflated count data. Ecol Modell 157: 179–188.
- 36. Smith JM, Macleod CD, Valavanis V, Hastie L, Valinassab T, Bailey N, et al. (2013) Habitat and distribution of post-recruit life stages of the squid Loligo forbesii. Deep Sea Res Part II Top Stud Oceanogr 95: 145–159.
- 37. Ciannelli L, Chan K-S, Bailey KM, Stenseth NC (2004) Nonadditive effects of the environment on the survival of a large marine fish population. Ecology 85: 3418–3427.
- 38. R Core Team (2014) R: A language and environment for statistical computing. Available: http://www.r-project.org/.
- 39. Sánchez P, Maynou F, Demestre M (2004) Modelling catch, effort and price in a juvenile Eledone cirrhosa fishery over a 10-year period. Fish Res 68: 319–327.
- 40. Lloret J, Lleonart J, Sole I, Fromentin J-M (2001) Fluctuations of landings and environmental conditions in the north-western Mediterranean Sea. Fish Oceanogr 10: 33–50.
- 41. Quetglas A, Ordines F, Valls M (2011) What drives seasonal fluctuations of body condition in a semelparous income breeder octopus? Acta Oecologica 37: 476–483.
- 42. Lloret J, Palomera I, Salat J, Sole I (2004) Impact of freshwater input and wind on landings of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in shelf waters surrounding the Ebre (Ebro) River delta (north-western Mediterranean). Fish Oceanogr 13: 102–110.
- 43. Salat J (1996) Review of hydrographic environmental factors that may influence anchovy habitats in northwestern Mediterranean. Sci Mar 60: 21–32.
- 44. Pertierra JP, Sánchez P (2005) Distribution of four cephalopoda species along the Catalan coast (NW Mediterranean) using GIS techniques. Phuket Mar Biol Cent Res Bull 66: 283–289.
- 45. Fanelli E, Cartes JE, Papiol V (2012) Assemblage structure and trophic ecology of deep-sea demersal cephalopods in the Balearic basin (NW Mediterranean). Mar Freshw Res 63: 264.
- 46. Oguz T, Macias D, Garcia-Lafuente J, Pascual A, Tintore J (2014) Fueling plankton production by a meandering frontal jet: a case study for the alboran sea (Western mediterranean). PLoS One 9: e111482. pmid:25372789
- 47. Vargas-Yáñez M, Moya F, García-Martínez M, Rey J, González M, Zunino P (2009) Relationships between Octopus vulgaris landings and environmental factors in the northern Alboran Sea (Southwestern Mediterranean). Fish Res 99: 159–167.
- 48. Villanueva R, Quintana D, Petroni G, Bozzano A (2011) Factors influencing the embryonic development and hatchling size of the oceanic squid Illex coindetii following in vitro fertilization. J Exp Mar Bio Ecol 407: 54–62.
- 49. Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Freshw Res 55: 331–339.
- 50. Friedland KD, Stock C, Drinkwater KF, Link JS, Leaf RT, Shank BV, et al. (2012) Pathways between primary production and fisheries yields of large marine ecosystems. PLoS One 7: e28945. pmid:22276100
- 51. Dahlhoff ElP, Stillman JH, Menge BA (2002) Physiological Community Ecology: Variation in Metabolic Activity of Ecologically Important Rocky Intertidal Invertebrates Along Environmental Gradients. Integr Comp Biol 871: 862–871.
- 52. André J, Pecl GT, Semmens JM, Grist EPM (2008) Early life-history processes in benthic octopus: Relationships between temperature, feeding, food conversion, and growth in juvenile Octopus pallidus. J Exp Mar Bio Ecol 354: 81–92.
- 53. Otero J, Álvarez-Salgado X, González A, Gilcoto M, Guerra Á (2009) High-frequency coastal upwelling events influence Octopus vulgaris larval dynamics on the NW Iberian shelf. Mar Ecol Prog Ser 386: 123–132.
- 54. Sveegaard S, Nabe-Nielsen J, Stæhr K, Jensen T, Mouritsen K, Teilmann J (2012) Spatial interactions between marine predators and their prey: herring abundance as a driver for the distributions of mackerel and harbour porpoise. Mar Ecol Prog Ser 468: 245–253.
- 55. Fauchald P, Erikstad KE (2002) Scale-dependent predator-prey interactions: The aggregative response of seabirds to prey under variable prey abundance and patchiness. Mar Ecol Prog Ser 231: 279–291.
- 56. Palomera I, Olivar MP, Salat J, Sabatés a., Coll M, García A, et al. (2007) Small pelagic fish in the NW Mediterranean Sea: An ecological review. Prog Oceanogr 74: 377–396.
- 57. Coll M, Palomera I, Tudela S, Sardà F (2006) Trophic flows, ecosystem structure and fishing impacts in the South Catalan Sea, Northwestern Mediterranean. J Mar Syst 59: 63–96.
- 58. Coll M, Palomera I, Tudela S, Dowd M (2008) Food-web dynamics in the South Catalan Sea ecosystem (NW Mediterranean) for 1978–2003. Ecol Modell 217: 95–116.
- 59. Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and Ecology of Species Range Limits. Annu Rev Ecol Evol Syst 40: 415–436.
- 60. Fernández de Puelles ML, Lopéz-Urrutia Á, Morillas A, Molinero JC (2008) Seasonal variability of copepod abundance in the Balearic region (Western Mediterranean) as an indicator of basin scale hydrological changes. Hydrobiologia 617: 3–16.
- 61. Fernández de Puelles ML, Alemany F, Jansá J (2007) Zooplankton time-series in the Balearic Sea (Western Mediterranean): Variability during the decade 1994–2003. Prog Oceanogr 74: 329–354.
- 62. Hidalgo M, Massutí E, Moranta J, Cartes J, Lloret J, Oliver P, et al. (2008) Seasonal and short spatial patterns in European hake (Merluccius merluccius L.) recruitment process at the Balearic Islands (western Mediterranean): The role of environment on distribution and condition. J Mar Syst 71: 367–384.
- 63. Hidalgo M, Tomás J, Moranta J, Morales-Nin B (2009) Intra-annual recruitment events of a shelf species around an island system in the NW Mediterranean. Estuar Coast Shelf Sci 83: 227–238.
- 64. Guijarro B, Massutí E, Moranta J, Díaz P (2008) Population dynamics of the red shrimp Aristeus antennatus in the Balearic Islands (western Mediterranean): Short spatio-temporal differences and influence of environmental factors. J Mar Syst 71: 385–402.
- 65. Balbín R, López-Jurado JL, Flexas MM, Reglero P, Vélez-Velchí P, González-Pola C, et al. (2014) Interannual variability of the early summer circulation around the Balearic Islands: Driving factors and potential effects on the marine ecosystem. J Mar Syst 138: 70–81.
- 66. Alemany F, Quintanilla L, Velez-Belchí P, García a., Cortés D, Rodríguez JM, et al. (2010) Characterization of the spawning habitat of Atlantic bluefin tuna and related species in the Balearic Sea (western Mediterranean). Prog Oceanogr 86: 21–38.
- 67. Torres AP, Reglero P, Balbin R, Urtizberea A, Alemany F (2011) Coexistence of larvae of tuna species and other fish in the surface mixed layer in the NW Mediterranean. J Plankton Res 33: 1793–1812.
- 68. Balbín R, Flexas MM, López-Jurado JL, Peña M, Amores a., Alemany F (2012) Vertical velocities and biological consequences at a front detected at the balearic sea. Cont Shelf Res 47: 28–41.
- 69. Field JC, Baltz K, Phillips AJ, Walker WA (2007) Range expansion and trophic interactions of the jumbo squid, Dosidicus gigas, in the California current. CalCOFI Reports 48: 131–146.
- 70. Zeidberg LD, Robison BH (2007) Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proc Natl Acad Sci USA 104: 12948–12950. pmid:17646649
- 71. Pecl GT, Jackson GD (2008) The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Rev Fish Biol Fish 18: 373–385.
- 72. Calvo E, Simó R, Coma R, Ribes M, Pascual J, Sabatés A, et al. (2011) Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Clim Res 50: 1–29.
- 73. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc Natl Acad Sci USA 106: 6176–6181. pmid:19332777
- 74. Albouy C, Velez L, Coll M, Colloca F, Le Loc’h F, Mouillot D, et al. (2014) From projected species distribution to food-web structure under climate change. Glob Chang Biol 20: 730–741. pmid:24214576
- 75. Sabatés a., Olivar MP, Salat J, Palomera I, Alemany F (2007) Physical and biological processes controlling the distribution of fish larvae in the NW Mediterranean. Prog Oceanogr 74: 355–376.