Biodiversity and global change in Mediterranean benthic communities: perspectives over large spatial and long temporal scales

Many terrestrial and marine systems are experiencing accelerating decline due to the effects of global change. This situation has raised concern about the consequences of biodiversity losses for ecosystem function, ecosystem service provision, and human well-being. Coastal marine habitats are a main focus of attention because they harbour a high biological diversity, are among the most productive systems of the world and present high anthropogenic interaction levels. The accelerating degradation of many terrestrial and marine systems highlights the urgent need to evaluate the consequence of biodiversity loss. Because marine biodiversity is a dynamic entity and this study was interested global change impacts, this study focused on benthic biodiversity trends over large spatial and long temporal scales. The main aim of this project was to investigate the current extent of biodiversity of the high diverse benthic coralligenous community in the Mediterranean Sea, detect its changes, and predict its future changes over broad spatial and long temporal scales. These marine communities are characterized by structural species with low growth rates and long life spans; therefore they are considered particularly sensitive to disturbances. For this purpose, this project analyzed permanent photographic plots over time at four locations in the NW Mediterranean Sea. The spatial scale of this study provided information on the level of species similarity between these locations, thus offering a solid background on the amount of large scale variability in coralligenous communities; whereas the temporal scale was fundamental to determine the natural variability in order to discriminate between changes observed due to natural factors and those related to the impact of disturbances (e.g. mass mortality events related to positive thermal temperatures, extreme catastrophic events). This study directly addressed the challenging task of analyzing quantitative biodiversity data of these high diverse marine benthic communities. Overall, the scientific knowledge gained with this research project will improve our understanding in the function of marine ecosystems and their trajectories related to global change.

Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in northwest Mediterranean

Temporal variability was studied in the common sea urchin Paracentrotus lividus through the analysis of the genetic composition of three yearly cohorts sampled over two consecutive springs in a locality in northwestern Mediterranean. Individuals were aged using growth ring patterns observed in tests and samples were genotyped for five microsatellite loci. No reduction of genetic diversity was observed relative to a sample of the adult population from the same location or within cohorts across years. FST and amova results indicated that the differentiation between cohorts is rather shallow and not significant, as most variability is found within cohorts and within individuals. This mild differentiation translated into estimates of effective population size of 90100 individuals. When the observed excess of homozygotes was taken into account, the estimate of the average number of breeders increased to c. 300 individuals. Given our restricted sampling area and the known small-scale heterogeneity in recruitment in this species, our results suggest that at stretches of a few kilometres of shoreline, large numbers of progenitors are likely to contribute to the larval pool at each reproduction event. Intercohort variation in our samples is six times smaller than spatial variation between adults of four localities in the western Mediterranean. Our results indicate that, notwithstanding the stochastic events that take place during the long planktonic phase and during the settlement and recruitment processes, reproductive success in this species is high enough to produce cohorts genetically diverse and with little differentiation between them. Further research is needed before the link between genetic structure and underlying physical and biological processes can be well established.

An introduction to Mediterranean deep-sea biology

This chapter presents the state of the art concerning the deep-sea Mediterranean environment: geology, hydrology, biology and fisheries. These are the fields of study dealt with in the scientific papers of this volume. The authors are specialists who have addressed their research to the Mediterranean deep-sea environment during the last years. This introduction is an overview but not an exhaustive review.

Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs

We annually monitored the abundance and size structure of herbivorous sea urchin populations (Paracentrotus lividus and Arbacia lixula) inside and outside a marine reserve in the Northwestern Mediterranean on two distinct habitats (boulders and vertical walls) over a period of 20 years, with the aim of analyzing changes at different temporal scales in relation to biotic and abiotic drivers. P. lividus exhibited significant variability in density over time on boulder bottoms but not on vertical walls, and temporal trends were not significantly different between the protection levels. Differences in densities were caused primarily by variance in recruitment, which was less pronounced inside the MPA and was correlated with adult density, indicating density-dependent recruitment under high predation pressure, as well as some positive feedback mechanisms that may facilitate higher urchin abundances despite higher predator abundance. Populations within the reserve were less variable in abundance and did not exhibit the hyper-abundances observed outside the reserve, suggesting that predation effects maybe more subtle than simply lowering the numbers of urchins in reserves. A. lixula densities were an order of magnitude lower than P. lividus densities and varied within sites and over time on boulder bottoms but did not differ between protection levels. In December 2008, an exceptionally violent storm reduced sea urchin densities drastically (by 50% to 80%) on boulder substrates, resulting in the lowest values observed over the entire study period, which remained at that level for at least two years (up to the present). Our results also showed great variability in the biological and physical processes acting at different temporal scales. This study highlights the need for appropriate temporal scales for studies to fully understand ecosystem functioning, the concepts of which are fundamental to successful conservation and management.

The population dynamics of Halecium petrosum and Halecium pusillum (Hydrozoa, Cnidaria), epiphytes of Halimeda tuna in the nortwestern Mediterranean

Halecium petrosum and Halecium pusillum on the alga Halimeda tuna from Tossa de Mar, northeastern Spain, were studied. Asexual reproduction of H. petrosum, by stolonisation, occurred throughout the year except for July and August. Asexual reproduction of H. pusillum, by planktonic propagules, occurred throughout the year. Sexual reproduction was limited to the autumn in H. petrosum and spring in H. pusillum. The growth rates of colonies of both species were rapid but declined with increased size. Mean colony size over two consecutive two week periods increased approximately five-fold and three-fold for H. petrosum, and six-fold and four-fold for H. pusillum. Mortality was estimated to be high for both species, especially in summer. The maximum life span of colonies (ramets) of both species was estimated to be only eight weeks. Consequently most colonies do not reproduce sexually. The absence of reproduction of H. petrosum in summer, when the turnover of algal thalli was greatest, probably contributed to the summer decline in its abundance. In both species the genet (clone) survives for unknown, possibly very long, periods by asexual reproduction which facilites colonisation of other substrata.

'Heures' a bio-economic model for Mediterranean fisheries, towards the evaluation of management strategies

The bio-economic model "Heures" is a first attempt to develop a simulation procedure to understand the Northwestern Mediterranean fisheries, to evaluate management strategies and to analyze the feasibility of implementing an adaptative management. The model is built on the interaction among three boxes simulating the dynamics of each of the basic actors of a fishery: the stock, the market and the fishermen. A fourth actor, the manager, imposes or modifies the rules, or, in terms of the model, modifies some particular parameters. Thus, the model allows us to simulate and evaluate the mid-term biologic and economic effects of particular management measures. The bio-economic nature of the model is given by the interaction among the three boxes, by the market simulation and, particularly, by the fishermen behaviour. This last element confers to the model its Mediterranean"selfregulated" character. The fishermen allocate their investments to maximize fishing mortality but, having a legal effort limit, they invest in maintenance and technology in order to increase the catchability, which, as a consequence. will be function of the invested capital.

A bioeconomic model for Mediterranean fisherires, the hake off Catalonia (western Mediterranean) as a case study

The theoretical aspects and the associated software of a bioeconomic model for Mediterranean fisheries are presented. The first objective of the model is to reproduce the bioeconomic conditions in which the fisheries occur. The model is, perforce, multispecies and multigear. The main management procedure is effort limitation. The model also incorporates the usual fishermen strategy of increasing efficiency to obtain increased fishing mortality while maintaining the nominal effort. This is modelled by means of a function relating the efficiency (or technological progress) with the capital invested in the fishery and time. A second objective is to simulate alternative management strategies. The model allows the operation of technical and economic management measures in the presence of different kind of events. Both deterministic and stochastic simulations can be performed. An application of this tool to the hake fishery off Catalonia is presented, considering the other species caught and the different gears used. Several alternative management measures are tested and their consequences for the stock and economy of fishermen are analysed.

Tagging reveals limited exchange of immature loggerhead sea turtles (Caretta caretta) between regions in the western Mediterranean.

Exchange of immature loggerhead sea turtles (Caretta caretta) between the northern and southern regions of the western Mediterranean was investigated using data obtained from several Spanish tagging programmes. Tagged turtles ranged in straight carapace length from 23.0 to 74.0 cm. Thirty-six turtles were recaptured after an average interval of 390.5±462.6 days (SD). As the mean dispersal distance (MDD) of a turtle population that spreads over the western Mediterranean would stabilize after 117 days (CI 95%: 98 to 149), two analyses were conducted that included data from turtles recaptured after 98 and 149 days respectively. In both analyses, turtles were recaptured more often than expected in the same region where they had been tagged. No difference was found in either of the two regions between the average distance between the capture and recapture locations and the expected MDD if the turtles were to remain in the region where they were first captured. Turtles recaptured after 15 and 25 days respectively were excluded from the analysis to ensure data independence. The overall evidence indicates that immature turtles exhibit strong site fidelity to certain areas and that there is a strong barrier to dispersal between the northern and southern parts of the western Mediterranean. Therefore, loggerhead turtles in the western Mediterranean should be split into at least two management units.

Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs

We annually monitored the abundance and size structure of herbivorous sea urchin populations (Paracentrotus lividus and Arbacia lixula) inside and outside a marine reserve in the Northwestern Mediterranean on two distinct habitats (boulders and vertical walls) over a period of 20 years, with the aim of analyzing changes at different temporal scales in relation to biotic and abiotic drivers. P. lividus exhibited significant variability in density over time on boulder bottoms but not on vertical walls, and temporal trends were not significantly different between the protection levels. Differences in densities were caused primarily by variance in recruitment, which was less pronounced inside the MPA and was correlated with adult density, indicating density-dependent recruitment under high predation pressure, as well as some positive feedback mechanisms that may facilitate higher urchin abundances despite higher predator abundance. Populations within the reserve were less variable in abundance and did not exhibit the hyper-abundances observed outside the reserve, suggesting that predation effects maybe more subtle than simply lowering the numbers of urchins in reserves. A. lixula densities were an order of magnitude lower than P. lividus densities and varied within sites and over time on boulder bottoms but did not differ between protection levels. In December 2008, an exceptionally violent storm reduced sea urchin densities drastically (by 50% to 80%) on boulder substrates, resulting in the lowest values observed over the entire study period, which remained at that level for at least two years (up to the present). Our results also showed great variability in the biological and physical processes acting at different temporal scales. This study highlights the need for appropriate temporal scales for studies to fully understand ecosystem functioning, the concepts of which are fundamental to successful conservation and management.

A wolf in sheep"s clothing: carnivory in dominant sea urchins in the Mediterranean

Arbacia lixula and Paracentrotus lividus are the dominant sea urchins in the Mediterranean sublittoral, where they are key structuring species due to their grazing activity. It has been commonly accepted that competition between both species is minimized by specializing in different algal foods. A. lixula is considered to feed mainly on encrusting coralline algae, while P. lividus prefers fleshy macroalgae. We used stable isotope analysis to test if these species occupy different trophic positions at 3 locations in the western Mediterranean and one in Macaronesia. Our results show unambiguously that A. lixula always occupies a higher trophic level than P. lividus, with a δ15N comparable in some locations to strict carnivores such as Actinia schmidti or Marthasterias glacialis. A temporal monitoring at one locality showed that this signature of a higher trophic level is consistent throughout the year. These results are incompatible with the current belief of an herbivorous diet for A. lixula and suggest that it must be considered an omnivore tending to carnivory in Mediterranean ecosystems, feeding at least partially on sessile animals such as Cirripedia, Hydrozoa or Bryozoa. A parallel analysis of gut contents showed a predominance of vegetal items in both species, although A. lixula consistently had a higher abundance of animal components than P. lividus. Our results challenge the validity of using gut content observations alone for characterizing the trophic behaviour of omnivorous marine invertebrates that feed on a variety of food sources with different digestibility.

Natural or naturalized? phylogeography suggests that the abundant sea urchin arbacia lixula Is a recent Colonizer of the Mediterranean

We present the global phylogeography of the black sea urchin Arbacia lixula, an amphi-Atlantic echinoid with potential to strongly impact shallow rocky ecosystems. Sequences of the mitochondrial cytochrome c oxidase gene of 604 specimens from 24 localities were obtained, covering most of the distribution area of the species, including the Mediterranean and both shores of the Atlantic. Genetic diversity measures, phylogeographic patterns, demographic parameters and population differentiation were analysed. We found high haplotype diversity but relatively low nucleotide diversity, with 176 haplotypes grouped within three haplogroups: one is shared between Eastern Atlantic (including Mediterranean) and Brazilian populations, the second is found in Eastern Atlantic and the Mediterranean and the third is exclusively from Brazil. Significant genetic differentiation was found between Brazilian, Eastern Atlantic and Mediterranean regions, but no differentiation was found among Mediterranean sub-basins or among Eastern Atlantic sub-regions. The star-shaped topology of the haplotype network and the unimodal mismatch distributions of Mediterranean and Eastern Atlantic samples suggest that these populations have suffered very recent demographic expansions. These expansions could be dated 94-205 kya in the Mediterranean, and 31-67 kya in the Eastern Atlantic. In contrast, Brazilian populations did not show any signature of population expansion. Our results indicate that all populations of A. lixula constitute a single species. The Brazilian populations probably diverged from an Eastern Atlantic stock. The present-day genetic structure of the species in Eastern Atlantic and the Mediterranean is shaped by very recent demographic processes. Our results support the view (backed by the lack of fossil record) that A. lixula is a recent thermophilous colonizer which spread throughout the Mediterranean during a warm period of the Pleistocene, probably during the last interglacial. Implications for the possible future impact of A. lixula on shallow Mediterranean ecosystems in the context of global warming trends must be considered.

Time and space: genetic structure of the common sea urchin paracentrotus lividus in the south-eastern iberian coast

Spatio-temporal variability in settlement and recruitment, high mortality during the first life-history stages, and selection may determine the genetic structure of cohorts of long-lived marine invertebrates at small scales. We conducted a spatial and temporal analysis of the common Mediterranean Sea urchin Paracentrotus lividus to determine the genetic structure of cohorts at different scales. In Tossa de Mar (NW Mediterranean), recruitment was followed over 5 consecutive springs (2006-2010). In spring 2008, recruits and two-year-old individuals were collected at 6 locations along East and South Iberian coasts separated from 200 to over 1,100 km. All cohorts presented a high genetic diversity based on a fragment of mtCOI. Our results showed a marked genetic homogeneity in the temporal monitoring and a low degree of spatial structure in 2006. In 2008, coupled with an abnormality in the usual circulation patterns in the area, the genetic structure of the southern populations studied changed markedly, with arrival of many private haplotypes. This fact highlights the importance of point events in renewing the genetic makeup of populations, which can only be detected through analysis of the cohort structure coupling temporal and spatial perspectives.

The reproductive cycle of the sea urchin Arbacia lixula in northwest mediterranean: potential influence of temperature and photoperiod

We studied the reproductive cycle of the sea urchin Arbacia lixula in a subtidal population from northeast Spain over four years using a gonadosomatic index (GSI) and gonad histology. Our results show that the GSI of A. lixula follows a seasonal cycle which peaks in May-July and attains its lowest values in October-November every year. The time course of the GSI matched closely the photoperiod cycle. We also found a remarkable inter-annual variability in the maximum value of GSI, which correlated with mean water temperature during the gonad growth period (winter and spring). Gonad histology was also in agreement with a single gametogenic cycle per year in this species. We explored the application of circular statistics to present and analyse gonadal development data, which allowed us to adequately handle the high intra-individual variability detected, with several developmental stages commonly found within the same gonad. The picture that emerged is one of a gametogenic timing driven by photoperiod, while the amount of reproductive output is determined by temperature. This is coherent with the tropical origin of the species and lends support to recent warnings about an increase in the abundance of this species in the Mediterranean as a result of global warming, with associated increased impact potential in sublittoral communities.

Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs

We annually monitored the abundance and size structure of herbivorous sea urchin populations (Paracentrotus lividus and Arbacia lixula) inside and outside a marine reserve in the Northwestern Mediterranean on two distinct habitats (boulders and vertical walls) over a period of 20 years, with the aim of analyzing changes at different temporal scales in relation to biotic and abiotic drivers. P. lividus exhibited significant variability in density over time on boulder bottoms but not on vertical walls, and temporal trends were not significantly different between the protection levels. Differences in densities were caused primarily by variance in recruitment, which was less pronounced inside the MPA and was correlated with adult density, indicating density-dependent recruitment under high predation pressure, as well as some positive feedback mechanisms that may facilitate higher urchin abundances despite higher predator abundance. Populations within the reserve were less variable in abundance and did not exhibit the hyper-abundances observed outside the reserve, suggesting that predation effects maybe more subtle than simply lowering the numbers of urchins in reserves. A. lixula densities were an order of magnitude lower than P. lividus densities and varied within sites and over time on boulder bottoms but did not differ between protection levels. In December 2008, an exceptionally violent storm reduced sea urchin densities drastically (by 50% to 80%) on boulder substrates, resulting in the lowest values observed over the entire study period, which remained at that level for at least two years (up to the present). Our results also showed great variability in the biological and physical processes acting at different temporal scales. This study highlights the need for appropriate temporal scales for studies to fully understand ecosystem functioning, the concepts of which are fundamental to successful conservation and management.

Low Dynamics, High Longevity and Persistence of Sessile Structural Species Dwelling on Mediterranean Coralligenous Outcrops

There is still limited understanding of the processes underlying benthic species dynamics in marine coastal habitats, which are of disproportionate importance in terms of productivity and biodiversity. The life-history traits of long-lived benthic species in these habitats are particularly poorly documented. In this study, we assessed decadal patterns of population dynamics for ten sponge and anthozoan species that play key structural roles in coralligenous outcrops (~25 m depth) in two areas of the NW Mediterranean Sea. This study was based on examination of a unique long-term photographic series, which allowed analysis of population dynamics over extensive spatial and time spans for the very first time. Specifically, 671 individuals were censused annually over periods of 25-, 15-, and 5-years. This long-term study quantitatively revealed a common life-history pattern among the ten studied species, despite the fact they present different growth forms. Low mortality rates (3.4% yr−1 for all species combined) and infrequent recruitment events (mean value of 3.1±0.5 SE recruits yr−1) provided only a very small fraction of the new colonies required to maintain population sizes. Overall, annual mortality and recruitment rates did not differ significantly among years; however, some species displayed important mortality events and recruitment pulses, indicating variability among species. Based on the growth rates of these 10 species, we projected their longevity and, obtained a mean estimated age of 25-200 years. Finally, the low to moderate turnover rates (mean value 0.80% yr−1) observed among the coralligenous species were in agreement with their low dynamics and persistence. These results offer solid baseline data and reveal that these habitats are among the most vulnerable to the current increases of anthropogenic disturbances.