Why coastal lagoons are so productive? Physical bases of fishing productivity in coastal lagoons.

Coastal lagoons are among the most productive marine ecosystems in the world. Annual primary production varies from 50 to > 500 g C m-2 year-1, being of the same order of magnitude as that of the upwelling areas. Many lagoons lie within the range of eutrophic (300-500 g C m-2 year-1) or hypereutrophic (> 500 g C m-2 year-1) conditions. The high productivity of coastal lagoons makes them subject of exploitation by many marine fishes and invertebrates, that use them as nursery areas and feeding grounds during their early life cycle phases, and most lagoons support important fisheries or maintain aquaculture exploitations. The high levels of their biological production can be explained by some of their common features as shallowness and the strong influence of terrestrial systems. Shallowness favors that the photic zone extends to the lagoon bottom and that wind can promote the resuspension of nutrients and organisms. The interaction with land also introduces significant amounts of nutrients. However, trophic variables can explain < 43 % of the fishing yields, and further than the trophic status of the lagoons, several works showed that the biological productivity of coastal lagoons can be explained by their geomorphological features such as the positive influence of shoreline development and the negative influence of depth. Using the Mar Menor lagoon as a case study, we propose that although nutrient inputs and light can be limiting factors for photosynthetic based productivity, increasing fishing yield up to a certain limit, the productivity of lagoons is mainly promoted by more general forces associated to physical and chemical gradients.

Long-term sediment records reveal over three thousand years of heavy metal inputs in the Mar Menor coastal lagoon (SE Spain).

The Mar Menor lagoon combined high biological production and environmental quality, making it an important economic engine. However, the pressure of human activities put its ecological integrity at risk, the oldest environmental impact being mining activity recorded since Roman times, about 3500 years ago, reaching its maximum intensity in the 20th century, contributing heavy metals to the lagoon sediments for almost 30 centuries. This work reviews the spatiotemporal evolution of the main heavy metals in this coastal lagoon using data from 272 surface sediment samples obtained during the last 40 years and two deep cores covering the total history of the lagoon (c. 6500 yrs BP), so as their incidence in the lagoon trophic web. The observed patterns in sedimentation, sediment characteristics and heavy metal content respond to the complex interaction, sometimes synergistic and sometimes opposing, between climatic conditions, biological production and human activities, with mining being mainly responsible for Pb, Zn and Cd inputs and port activities for Cu. High Fe/Al, Ti/Al and Zr/Al ratios identify periods of mining activity, while periods of arid climatic conditions and deforestation that increase erosion processes in the drainage basin and silt concentration in the lagoon sediments are determined by high Zr/Rb and, to a lesser extent, Zr/Al and Si/Al ratios. After the cessation of direct discharges into the lagoon in the 1950s, the recent evolution of heavy metals concentration and its spatial redistribution would be determined by hydrographic and biogeochemical processes, solubility of different elements, and coastal works in harbours and on beaches. The bioconcentration factor decreases along the trophic levels of the food web, suggesting that the lagoon ecosystem provides an important service by retaining heavy metals in the sediment, largely preventing their bioavailability, but actions involving resuspension or changes in sediment conditions would pose a risk to organisms.

Phenology of scyphozoan jellyfish species in a eutrophication and climate change context.

The uprising interest in gelatinous zooplankton populations must cope with a lack of robust time series of direct abundance observations in most of the ecosystems because of the difficulties in sampling small, fragile organisms, and of the dismissal of jellyfish as a nuisance. Most of the hypotheses about their dynamics are built on a few species and ecosystems and extended to the whole group, but the blooms are registered mainly for the members of the Class Scyphozoa that dwell in temperate, shallow waters. Within the scyphozoans, our knowledge about their phenology relies mainly on laboratory experiences. Here we present a long-term analysis of the phenology and life cycle of three scyphozoan species in an ecosystem affected by eutrophication in a climate change context. We have found that the phenology is directed by temperature, but not modified by different thermal and ecological regimes.

Recolonization origin and reproductive locations, but not isolation from the sea, lead to genetic structure in migratory lagoonal fishes.

The assessment of connectivity in marine ecosystems is a requirement to adequate fisheries management. In this study we have selected two commercially exploited migratory species, European perch (Perca fluviatilis) and European smelt (Osmerus eperlanus), to evaluate the connectivity between the Curonian Lagoon and the coastal Baltic Sea. Our results indicate that isolation between the coastal lagoon and the adjacent sea area does not lead to the formation of genetic structure in migratory fish species. However, both species do register subpopulations coexisting in the area without interbreeding. This indicates that the fisheries management for migratory fishes in coastal lagoons affects a wider area than just the coastal lagoon. European perch, being a postglacial recolonizer from various refugees, has four different subpopulations, while the mechanism that maintains this division remains unexplored. The feeding migrations of European perch to the coastal zone suggest that the reproduction might occur elsewhere and that the factors for genetic structure suggested at the Baltic Sea scale might operate during these migrations. For European smelt, we discuss the existence of two different ecotypes, one lagoonal and one diadromous, and the different registered spawning locations as explicative causes for the maintenance of two genetically divergent clusters. The lagoonal ecotype reproduces and spawns inside the Curonian Lagoon while the diadromous one lives in the open Baltic Sea, performing spawning migrations to the lagoon and the mouth of Nemunas river, thus, maintaining the genetic divergence among them. However, our results indicate that there are no differences in size between both clusters, while the lagoonal population is expected to be smaller, forbidding the determination of two genetically different ecotypes. We conclude that there are no geographically and genetically separated populations of these two species in the lagoon-sea- terrestrial inlets continuum, and unified stock management for the coastal Baltic Sea and the Curonian lagoon is required.

Nutrient overload promotes the transition from top-down to bottom-up control and triggers dystrophic crises in a Mediterranean coastal lagoon.

The excess input of nutrients that triggers eutrophication processes is one of the main destabilizing factors of coastal ecosystems, being coastal lagoons prone to suffer these effects and present dystrophic crises. This process is aggravated by the current trend of rising temperatures and more frequent torrential rains due to climate change. We observed that the Mar Menor lagoon had a great capacity for self-regulation of its trophic web and resistance to the eutrophication process, but after 30 years of nutrient input due to the change in the agricultural regime in its drainage basin in the 1990s, the lagoon ecosystem has suffered several of these events. In this work, we characterize the seasonal dynamic of the pelagic system during the last dystrophic crises. Phosphorus and nitrogen alternate as the limiting nutrient for phytoplankton proliferation. The entrance of phosphorus is mainly related to vacation periods, while nitrogen inputs, both superficial and sub-superficial, are more related to chronic high nitrates concentration in the water table after the agricultural activities carried out in the area changed. Our analysis reveals that the summer season is prone to suffer periodical hypoxia events when the N/P ratio decreases, and the temperature rises. In the Mar Menor, the ecological balance has been maintained in recent decades thanks to, among other mechanisms, the spatial and temporal segregation of top-down control over phytoplankton exerted by three species of jellyfish. However, the deep reduction in the abundance of the summer jellyfish species and the excessive proliferation of phytoplankton has meant the loss of this control. Moreover, we have registered a decline in the abundance of all the other zooplanktonic groups during the dystrophic crises. We suggest that management actions should address the input sources of water and nutrients, and an integrated management of the activities carried out throughout the watershed.

Larger scyphozoan species dwelling in temperate, shallow waters show higher blooming potential.

142 scientific publications have been reviewed on the characteristics of the scyphozoans with respect to their ability to develop blooms and the most significant environmental characteristics that determine them. Special attention was paid to depth, temperature, salinity, chlorophyll concentration, and the habitat of the 39 registered blooming genera. After the review, we find that over the past decades, the number of scyphozoan blooming-species is higher than previously recorded, increasing from circa 14% to 25% of the class. Species that inhabit depths less than 27.1 m are prone to produce blooms, particularly in semienclosed areas with low rates of water renewal and high thermal amplitudes. Temperature appears as the main environmental factor controlling blooms, but food availability is essential to sustain the proliferations. Interspecies variability in the response to environmental factors observed in this work suggest that bloom predictive models should be constructed species-habitat-specific.

New genomic resources for three exploited Mediterranean fishes.

Extensive fishing has led to fish stock declines throughout the last decades. While clear stock identification is required for designing management schemes, stock delineation is problematic due to generally low levels of genetic structure in marine species. The development of genomic resources can help to solve this issue. Here, we present the first mitochondrial and nuclear draft genome assemblies of three economically important Mediterranean fishes, the white seabream, the striped red mullet, and the comber. The assemblies are between 613 and 785 Mbp long and contain between 27,222 and 32,375 predicted genes. They were used as references to map Restriction-site Associated DNA markers, which were developed with a single-digest approach. This approach provided between 15,710 and 21,101 Single Nucleotide Polymorphism markers per species. These genomic resources will allow uncovering subtle genetic structure, identifying stocks, assigning catches to populations and assessing connectivity. Furthermore, the annotated genomes will help to characterize adaptive divergence.

Can an oligotrophic coastal lagoon support high biological productivity? Sources and pathways of primary production.

Coastal lagoons are among the most productive systems in the world. Many marine species make use of this by entering the lagoons as juveniles for nursery and growth before returning to the sea for reproduction. Humans take advantage of such fish migration processes by fishing, and exploit the high productivity for aquaculture activities. The Mar Menor is one of the largest coastal lagoons in the Mediterranean, sustaining relatively high fishing intensity despite the fact that it has traditionally been characterized as highly oligotrophic. However, in the last decades, this lagoon has suffered drastic changes induced by human activities. This has led to eutrophication, which started mainly as a consequence of changes in agricultural practices in the lagoon watershed, and triggered such fundamental changes in the system, as the mass development of jellyfish. The aim of this work is to capture and analyse the structure and functioning of the trophic web of the Mar Menor when it was still, in contrast to other coastal lagoons, oligotrophic, to provide a start point for analysing the consequences of changes in the distribution of macrophyte meadows and of eutrophication. We have compiled a detailed trophic model of this lagoon, comprising 94 compartments, using an ECOPATH model to capture the period 1980-1995. At this time the lagoon was an autotrophic system with a high net surplus of production that reached 9124.31gC/m2/year, while the production/biomass (P/B) ratio reached 34.56 and the total primary production/total respiration ratio was 7.01. The lagoon exported a 38.46% of total flows, including the catch by fishing, and 44.40% went to detritus. The primary production was mainly benthic (99.4%) due to the microphytobenthos and macrophytes. However, despite the fact that total fishery landings in the study period ranged between 144,835.5 and 346,708.5 kg, the gross efficiency was low, making up only 0.005% of the net primary production. This could partly be explained by the high trophic level of the fish catch (2.9), but mainly because most of the primary production (10,532.06 gC/m2/year) went directly to the detritus pool and was accumulated in the sediment in the Caulerpa prolifera meadows. We suggest several reasons why such high productivity coincided with low chlorophyll concentrations and good overall water quality: 1) the domination of both benthic biomass and primary production over pelagic ones with a high biomass of filter feeders, detritus feeders and scavengers, 2) high species diversity, complex and long food webs characterized by low connectance,3) the export of a significant part of the production from the system, and 4) the accumulation of surplus organic matter (as detritus) in sediments. We compare the food web of the Mar Menor in this mentioned oligotrophic stage to those of ten other lagoons in pursuit of more general implications regarding lagoon ecosystem functioning.

Long-Distance Benefits of Marine Reserves: Myth or Reality?

Long-distance (>40-km) dispersal from marine reserves is poorly documented; yet, it can provide essential benefits such as seeding fished areas or connecting marine reserves into networks. From a meta-analysis, we suggest that the spatial scale of marine connectivity is underestimated due to the limited geographic extent of sampling designs. We also found that the largest marine reserves (>1000km2) are the most isolated. These findings have important implications for the assessment of evolutionary, ecological, and socio-economic long-distance benefits of marine reserves. We conclude that existing methods to infer dispersal should consider the up-to-date genomic advances and also expand the spatial scale of sampling designs. Incorporating long-distance connectivity in conservation planning will contribute to increase the benefits of marine reserve networks.

Effect of marine protected areas on distinct fish life-history stages.

The role of Marine Protected Areas on distinct life stages of Mediterranean reef fish species (classified on the basis of their economic value and mobility categories) was assessed in a network of marine reserves in SE Spain. Only abundance and biomass of adult of both commercial and demersal species were positively affected by protection. Gradients across reserve boundaries (as a clue to the occurrence of spillover) were observed for fish abundance but not for biomass, indicating a protected fish assemblage with a predominance of small-sized individuals. Also, post-larvae of commercial species were negatively related to protected zones. Active selection of settlement preferred habitats, larval accumulation favoured by the geomorphological configuration of the coast or mixed effects has been proposed as possible explanations. Juveniles showed high spatial variability resulting in a lack of response to fishing protection measures. We highlight the need of including early life stages and overall suitable habitats for them when designing MPA networks due to the crucial importance of these stages to successful fulfillment of MPA objectives.

Use of Lagrangian simulations to hindcast the geographical position of propagule release zones in a Mediterranean coastal fish.

The study of organism dispersal is fundamental for elucidating patterns of connectivity between populations, thus crucial for the design of effective protection and management strategies. This is especially challenging in the case of coastal fish, for which information on egg release zones (i.e. spawning grounds) is often lacking. Here we assessed the putative location of egg release zones of the saddled sea bream (Oblada melanura) along the south-eastern coast of Spain in 2013. To this aim, we hindcasted propagule (egg and larva) dispersal using Lagrangian simulations, fed with species-specific information on early life history traits (ELTs), with two approaches: 1) back-tracking and 2) comparing settler distribution obtained from simulations to the analogous distribution resulting from otolith chemical analysis. Simulations were also used to assess which factors contributed the most to dispersal distances. Back-tracking simulations indicated that both the northern sector of the Murcia region and some traits of the North-African coast were hydrodynamically suitable to generate and drive the supply of larvae recorded along the coast of Murcia in 2013. With the second approach, based on the correlation between simulation outputs and field results (otolith chemical analysis), we found that the oceanographic characteristics of the study area could have determined the pattern of settler distribution recorded with otolith analysis in 2013 and inferred the geographical position of main O. melanura spawning grounds along the coast. Dispersal distance was found to be significantly affected by the geographical position of propagule release zones. The combination of methods used was the first attempt to assess the geographical position of propagule release zones in the Mediterranean Sea for O. melanura, and can represent a valuable approach for elucidating dispersal and connectivity patterns in other coastal species.

Conservation physiology of marine fishes: state of the art and prospects for policy.

The state of the art of research on the environmental physiology of marine fishes is reviewed from the perspective of how it can contribute to conservation of biodiversity and fishery resources. A major constraint to application of physiological knowledge for conservation of marine fishes is the limited knowledge base; international collaboration is needed to study the environmental physiology of a wider range of species. Multifactorial field and laboratory studies on biomarkers hold promise to relate ecophysiology directly to habitat quality and population status. The 'Fry paradigm' could have broad applications for conservation physiology research if it provides a universal mechanism to link physiological function with ecological performance and population dynamics of fishes, through effects of abiotic conditions on aerobic metabolic scope. The available data indicate, however, that the paradigm is not universal, so further research is required on a wide diversity of species. Fish physiologists should interact closely with researchers developing ecological models, in order to investigate how integrating physiological information improves confidence in projecting effects of global change; for example, with mechanistic models that define habitat suitability based upon potential for aerobic scope or outputs of a dynamic energy budget. One major challenge to upscaling from physiology of individuals to the level of species and communities is incorporating intraspecific variation, which could be a crucial component of species' resilience to global change. Understanding what fishes do in the wild is also a challenge, but techniques of biotelemetry and biologging are providing novel information towards effective conservation. Overall, fish physiologists must strive to render research outputs more applicable to management and decision-making. There are various potential avenues for information flow, in the shorter term directly through biomarker studies and in the longer term by collaborating with modellers and fishery biologists.

Follow-me: A new start-and-stop method for visual animal tracking in biology research.

Very frequently, research in biology and ethology requires visual tracking of live animals, such as insects, rodents and fish. The challenge is particularly difficult in the aquatic environment because of the light scattering effect of water: reflections and refractions, low contrast and resolution images, noise, and also due to the unpredictable animal behavior. This paper describes a new tracking method that is based in start and stop detection. When the animals stop or move very slowly, a precise tracker based on AdaBoost classifiers is applied. Otherwise, when they move faster, a more efficient process based on background detection is used. A control system is responsible for deciding which method should be used in each instant. The experimental results using sea cucumbers (Echinodermata, Holothuroidea), zebrafish and rodents, show the efficiency and accuracy of the proposed method, which is able to deal with complex situations.

Living in a coastal lagoon environment: photosynthetic and biochemical mechanisms of key marine macroalgae.

The physiological status of Cystoseira compressa, Padina pavonica and Palisada tenerrima was studied by in vivo chlorophyll fluorescence, pigment content, stoichiometry (C:N), accumulation of UV photoprotectors and antioxidant activity; comparing their photosynthetic response in a coastal lagoon (Mar Menor) and in Mediterranean coastal waters. In general, the specimens reached their highest ETRmax in spring in the Lagoon, but in summer in the Mediterranean, coinciding with their maximum biomass peak. The species exhibited a dynamic photoinhibition. Except C. compressa, they showed a lower decrease in Fv/Fm and higher recovery rates in the Mediterranean populations when exposed to high irradiance. The higher salinity and temperature of the lagoon could impair the photoprotection mechanisms. The acclimation to lagoon environments is species-specific and involves complex regulatory mechanisms. The results underline the importance of N in repair, avoidance, quenching and scavenging mechanisms. In general, Lagoon specimens showed higher pigment concentration. Although xanthophylls play important photo-protective and antioxidant roles, the observed trend is more likely to be explained by the higher temperatures reached in the lagoon compared to Mediterranean. Therefore the studied photosynthetic and biochemical mechanisms can be effective not only for high irradiance, but also for higher temperatures in a climate change scenario, but are highly dependent on nutrient availability.

Response of rocky reef top predators (Serranidae: Epinephelinae) in and around marine protected areas in the Western Mediterranean Sea.

Groupers species are extremely vulnerable to overfishing and many species are threatened worldwide. In recent decades, Mediterranean groupers experienced dramatic population declines. Marine protected areas (MPAs) can protect populations inside their boundaries and provide individuals to adjacent fishing areas through the process of spillover and larval export. This study aims to evaluate the effectiveness of six marine reserves in the Western Mediterranean Sea to protect the populations of three species of grouper, Epinephelus marginatus, Epinephelus costae and Mycteroperca rubra, and to understand in which circumstances MPAs are able to export biomass to neighbouring areas. All the studied MPAs, except one where no grouper was observed, were able to maintain high abundance, biomass and mean weight of groupers. Size classes were more evenly distributed inside than outside MPAs. In two reserves, biomass gradients could be detected through the boundaries of the reserve as an indication of spillover. In some cases, habitat structure appeared to exert a great influence on grouper abundance, biomass and mean individual weight, influencing the gradient shape. Because groupers are generally sedentary animals with a small home range, we suggest that biomass gradients could only occur where groupers attain sufficient abundance inside MPA limits, indicating a strongly density-dependent process.

Conservation physiology of marine fishes: advancing the predictive capacity of models.

At the end of May, 17 scientists involved in an EU COST Action on Conservation Physiology of Marine Fishes met in Oristano, Sardinia, to discuss how physiology can be better used in modelling tools to aid in management of marine ecosystems. Current modelling approaches incorporate physiology to different extents, ranging from no explicit consideration to detailed physiological mechanisms, and across scales from a single fish to global fishery resources. Biologists from different sub-disciplines are collaborating to rise to the challenge of projecting future changes in distribution and productivity, assessing risks for local populations, or predicting and mitigating the spread of invasive species.

Physiological response and photoacclimation capacity of Caulerpa prolifera (Forsskål) J.V. Lamouroux and Cymodocea nodosa (Ucria) Ascherson meadows in the Mar Menor lagoon (SE Spain).

The macroalga Caulerpa prolifera colonized the Mar Menor coastal lagoon after the enlargement of the main inlet in 1972, coexisting now with the previous Cymodocea nodosa meadows. The physiological response and the photoacclimation capacity of both species were studied. For this purpose in vivo chlorophyll a fluorescence, photoprotective mechanisms and oxidative stress were measured in both species in summer 2010 and exposure-recovery experiments were conducted to determine the acclimation capacity of both species. The results suggest that C. prolifera behaves as a shade-adapted species with a low photoprotective capacity, light being one of the main factors governing its distribution in the lagoon. The high photosynthetic capacity and lack of photoinhibition found in C. nodosa suggest that this species is highly photoprotected. It also possesses a high concentration of lutein and a high de-epoxidation degree, related to a much higher NPQ(max) value.

Molecular systematics of the genus Holothuria in the Mediterranean and Northeastern Atlantic and a molecular clock for the diversification of the Holothuriidae (Echinodermata: Holothuroidea).

This work investigates the systematics of the genus Holothuria in the Mediterranean Sea and Northeastern Atlantic in the light of a wider molecular phylogenetic hypothesis of Holothuriidae, and it also provides a time-scale for the family diversification using mitochondrial markers and the molecular clock hypothesis. The subgenera Holothuria and Roweothuria are retrieved as paraphyletic. At least four separate lineages, with quite different time frameworks were identified. There are at least three species with an apparent long evolutionary history, H. forskali, H. sanctori and H. impatiens and six species belonging to Holothuria, Roweothuria and Vaneyothuria, which have diverged relatively recently.

Genetic diversity and connectivity remain high in Holothuria polii (Delle Chiaje 1823) across a coastal lagoon-open sea environmental gradient.

Coastal lagoons represent habitats with widely heterogeneous environmental conditions, particularly as regards salinity and temperature, which fluctuate in both space and time. These characteristics suggest that physical and ecological factors could contribute to the genetic divergence among populations occurring in coastal lagoon and open-coast environments. This study investigates the genetic structure of Holothuria polii at a micro-geographic scale across the Mar Menor coastal lagoon and nearby marine areas, estimating the mitochondrial DNA variation in two gene fragments, cytochrome oxidase I (COI) and 16S rRNA (16S). Dataset of mitochondrial sequences was also used to test the influence of environmental differences between coastal lagoon and marine waters on population genetic structure. All sampled locations exhibited high levels of haplotype diversity and low values of nucleotide diversity. Both genes showed contrasting signals of genetic differentiation (non-significant differences using COI and slight differences using 16S, which could due to different mutation rates or to differential number of exclusive haplotypes. We detected an excess of recent mutations and exclusive haplotypes, which can be generated as a result of population growth. However, selective processes can be also acting on the gene markers used; highly significant generalized additive models have been obtained considering genetic data from 16S gene and independent variables such as temperature and salinity.

Spatial assessment of fishing effort around European marine reserves: implications for successful fisheries management.

We examined the spatial dynamic of artisanal fishing fleets around five European marine protected areas (MPAs) to derive general implications for the evaluation of MPAs as fisheries management tools. The coastal MPAs studied were located off France, Malta and Spain and presented a variety of spatial designs and processes of establishment. We developed a standardized methodology to define factors influencing effort allocation and to produce fishing effort maps by merging GIS with geostatistical modelling techniques. Results revealed that in most cases the factors "distance to the no-take", "water depth", and "distance to the port" had a significant influence on effort allocation by the fishing fleets. Overall, we found local concentration of fishing effort around the MPA borders. Thus, neglecting the pattern of fishing effort distribution in evaluating MPA benefits, such as spillover of biomass, could hamper sound interpretation of MPAs as fisheries management tools.