Luis Cardona

Massive Consumption of Gelatinous Plankton by Mediterranean Apex Predators

Stable isotopes of carbon and nitrogen were used to test the hypothesis that stomach content analysis has systematically overlooked the consumption of gelatinous zooplankton by pelagic mesopredators and apex predators. The results strongly supported a major role of gelatinous plankton in the diet of bluefin tuna (Thunnus thynnus), little tunny (Euthynnus alletteratus), spearfish (Tetrapturus belone) and swordfish (Xiphias gladius). Loggerhead sea turtles (Caretta caretta) in the oceanic stage and ocean sunfish (Mola mola) also primarily relied on gelatinous zooplankton. In contrast, stable isotope ratios ruled out any relevant consumption of gelatinous plankton by bluefish (Pomatomus saltatrix), blue shark (Prionace glauca), leerfish (Lichia amia), bonito (Sarda sarda), striped dolphin (Stenella caerueloalba) and loggerhead sea turtles (Caretta caretta) in the neritic stage, all of which primarily relied on fish and squid. Fin whales (Balaenoptera physalus) were confirmed as crustacean consumers. The ratios of stable isotopes in albacore (Thunnus alalunga), amberjack (Seriola dumerili), blue butterfish (Stromaeus fiatola), bullet tuna (Auxis rochei), dolphinfish (Coryphaena hyppurus), horse mackerel (Trachurus trachurus), mackerel (Scomber scombrus) and pompano (Trachinotus ovatus) were consistent with mixed diets revealed by stomach content analysis, including nekton and crustaceans, but the consumption of gelatinous plankton could not be ruled out completely. In conclusion, the jellyvorous guild in the Mediterranean integrates two specialists (ocean sunfish and loggerhead sea turtles in the oceanic stage) and several opportunists (bluefin tuna, little tunny, spearfish, swordfish and, perhaps, blue butterfish), most of them with shrinking populations due to overfishing.

Living Together but Remaining Apart: Atlantic and Mediterranean Loggerhead Sea Turtles (Caretta caretta) in Shared Feeding Grounds

Juvenile loggerhead sea turtles (Caretta caretta) from Atlantic nesting populations migrate into the western Mediterranean, where they share feeding grounds with turtles originating in the Mediterranean. In this scenario, male-mediated gene flow may lead to the homogenization of these distant populations. To test this hypothesis, we genotyped 7 microsatellites from 56 Atlantic individuals sampled from feeding grounds in the western Mediterranean and then compared the observed allele frequencies with published data of 112 individuals from Mediterranean nesting beaches. Mediterranean populations were found to be genetically differentiated from the Atlantic stock reaching the western Mediterranean (F(st) = 0.029, P < 0.001); therefore, the possible mating events between Atlantic and Mediterranean individuals are not sufficient to homogenize these 2 areas. The differentiation observed between these 2 areas demonstrates that microsatellites are sufficiently powerful for mixed stock analysis and that individual assignment (IA) tests can be performed in combination with mitochondrial DNA (mtDNA) analysis. In a set of 197 individuals sampled in western Mediterranean feeding grounds, 87% were robustly assigned to Atlantic or Mediterranean groups with the combined marker, as compared with only 52% with mtDNA alone. These findings provide a new approach for tracking the movements of these oceanic migrants and have strong implications for the conservation of the species.

The diet of pelagic loggerhead sea turtles ( Caretta caretta ) off the Balearic archipelago (western Mediterranean): relevance of long-line baits

Gut content and stable isotope analyses were used to investigate the feeding habits of loggerhead sea turtles ( Caretta caretta ) inhabiting the Balearic archipelago. Turtles caught in the pelagic realm (δ 13 C: -16.0±0.6‰ and δ 15 N: 8.5±0.9‰) and turtles caught on the continental shelf (δ 13 C: -16.7±0.6‰ and δ 15 N: 8.4±1.3‰) did not differ in their isotopic signatures, suggesting that their diets include the same prey types. A mixing model revealed that for the turtles here analysed, squid and the jellyfish Cotylorhiza tuberculata were the most relevant prey, although stomach contents analysis revealed that carnivorous jellyplankton, neuston, fish and other cephalopods were also consumed. Gut content analysis also indicated that most of the prey identified, including all fish and most cephalopods, were of pelagic origin. Thus, loggerhead sea turtles inhabiting central regions of the western Mediterranean appear to seldom exploit benthic prey, even while on the continental shelf.

Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size

We investigated the sex- and size-related differences in the diet of whale sharks from the Arabian Sea (north-western Indian Ocean) using carbon and nitrogen stable-isotope analyses in white muscle. The samples were collected during the commercial fishing season between April and May of 2001 in Veraval (Gujarat, India). The overall isotope signature was similar to that of the pelagic-neritic zooplanktivore Ilisha melastoma, which suggests that both species are feeding on similar prey. In whale sharks, a positive relationship was found between δ15N and δ13C. This, together with a significant enrichment of both heavy stable isotopes with total length indicates that the contribution to the diet of small fish and/or larger zooplankton of higher trophic level increases with the movement from offshore areas to coastal areas as they grow. Gender differences in the isotopic ratios were not statistically significant, but small sample size cannot rule out completely the existence of some degree of spatial or dietary segregation between sexes.

Geographic Patterns of Genetic Variation in a Broadly Distributed Marine Vertebrate: New Insights into Loggerhead Turtle Stock Structure from Expanded Mitochondrial DNA Sequences

Previous genetic studies have demonstrated that natal homing shapes the stock structure of marine turtle nesting populations. However, widespread sharing of common haplotypes based on short segments of the mitochondrial control region often limits resolution of the demographic connectivity of populations. Recent studies employing longer control region sequences to resolve haplotype sharing have focused on regional assessments of genetic structure and phylogeography. Here we synthesize available control region sequences for loggerhead turtles from the Mediterranean Sea, Atlantic, and western Indian Ocean basins. These data represent six of the nine globally significant regional management units (RMUs) for the species and include novel sequence data from Brazil, Cape Verde, South Africa and Oman. Genetic tests of differentiation among 42 rookeries represented by short sequences (380 bp haplotypes from 3,486 samples) and 40 rookeries represented by long sequences (∼800 bp haplotypes from 3,434 samples) supported the distinction of the six RMUs analyzed as well as recognition of at least 18 demographically independent management units (MUs) with respect to female natal homing. A total of 59 haplotypes were resolved. These haplotypes belonged to two highly divergent global lineages, with haplogroup I represented primarily by CC-A1, CC-A4, and CC-A11 variants and haplogroup II represented by CC-A2 and derived variants. Geographic distribution patterns of haplogroup II haplotypes and the nested position of CC-A11.6 from Oman among the Atlantic haplotypes invoke recent colonization of the Indian Ocean from the Atlantic for both global lineages. The haplotypes we confirmed for western Indian Ocean RMUs allow reinterpretation of previous mixed stock analysis and further suggest that contemporary migratory connectivity between the Indian and Atlantic Oceans occurs on a broader scale than previously hypothesized. This study represents a valuable model for conducting comprehensive international cooperative data management and research in marine ecology.

Isotopic evidence of limited exchange between Mediterranean and eastern North Atlantic fin whales

RATIONALE The relationship between stocks of fin whales inhabiting the temperate eastern North Atlantic and the Mediterranean Sea is subject to controversy. The use of chemical markers facilitates an alternative insight into population structure and potential borders between stocks because the two areas present dissimilar isotopic baselines. METHODS Baleen plates, composed of inert tissue that keeps a permanent chronological record of the isotopic value of body circulating fluids, were used to investigate connectivity and boundaries between the stocks. Values were determined by continuous flow isotope ratio mass spectrometry. RESULTS Stable isotopes confirm that, while the two subpopulations generally forage in well-differentiated grounds, some individuals with characteristic Atlantic values do penetrate into the Mediterranean Sea up to the northernmost latitudes of the region. As a consequence, the border between the two putative subpopulations may be not as definite as previous acoustic investigations suggested. The discriminant function obtained in this study may assist researchers to use baleen plate isotopic data to assign the origin of fin whales of uncertain provenance. CONCLUSIONS This study strengthens the stock subdivision currently accepted for management and conservation while recognizes a low level of exchange between the Mediterranean and temperate eastern North Atlantic subdivisions.

δ15N value does not reflect fasting in mysticetes.

The finding that tissue δ15N values increase with protein catabolism has led researchers to apply this value to gauge nutritive condition in vertebrates. However, its application to marine mammals has in most occasions failed. We investigated the relationship between δ15N values and the fattening/fasting cycle in a model species, the fin whale, a migratory capital breeder that experiences severe seasonal variation in body condition. We analyzed two tissues providing complementary insights: one with isotopic turnover (muscle) and one that keeps a permanent record of variations in isotopic values (baleen plates). In both tissues δ15N values increased with intensive feeding but decreased with fasting, thus contradicting the pattern previously anticipated. The apparent inconsistency during fasting is explained by the fact that a) individuals migrate between different isotopic isoscapes, b) starvation may not trigger significant negative nitrogen balance, and c) excretion drops and elimination of 15N-depleted urine is minimized. Conversely, when intensive feeding is resumed in the northern grounds, protein anabolism and excretion start again, triggering 15N enrichment. It can be concluded that in whales and other mammals that accrue massive depots of lipids as energetic reserves and which have limited access to drinking water, the δ15N value is not affected by fasting and therefore cannot be used as an indicatior of nutritive condition.

Overfishing of small pelagic fishes increases trophic overlap between immature and mature striped dolphins in the Mediterranean Sea.

The interactions among diet, ecology, physiology, and biochemistry affect N and C stable isotope signatures in animal tissues. Here, we examined if ecological segregation among animals in relation to sex and age existed by analyzing the signatures of δ15N and δ13C in the muscle of Western Mediterranean striped dolphins. Moreover, we used a Bayesian mixing model to study diet composition and investigated potential dietary changes over the last two decades in this population. For this, we compared isotope signatures in samples of stranded dolphins obtained during two epizootic events occurring in 1990 and 2007–2008. Mean δ13C values for females and males were not significantly different, but age-related variation indicated δ13C enrichment in both sexes, suggesting that females and males most likely fed in the same general areas, increasing their consumption of benthic prey with age. Enrichment of δ15N was only observed in females, suggesting a preference for larger or higher trophic level prey than males, which could reflect different nutritional requirements. δ13C values showed no temporal variation, although the mean δ15N signature decreased from 1990 to 2007–2008, which could indicate a dietary shift in the striped dolphin over the last two decades. The results of SIAR indicated that in 1990, hake and sardine together contributed to 60% on the diet of immature striped dolphins, and close to 90% for mature striped dolphins. Conversely, the diet of both groups in 2007–2008 was more diverse, as hake and sardine contributed to less than 40% of the entire diet. These results suggest a dietary change that was possibly related to changes in food availability, which is consistent with the depletion of sardine stocks by fishing.

Cascading effects of the flathead grey mullet Mugil cephalus in freshwater eutrophic microcosmos

Flathead grey mullet (Mugil cephalus L.) stocked in fish ponds were long considered to feed primarily on detritus. However, recent research has found that they obtain much of their food from plankton and that they have a detrimental effect on pond zooplankton and large phytoplankton, whilst enhancing small phytoplankton. It has been suggested that flathead grey mullet may also increase the internal phosphorus loading of the ecosystem, which would also increase phytoplankton density. To test whether zooplankton removal or nutrient release from the sediment is the better explanation for phytoplankton enhancement in the presence of flathead grey mullet, the ecosystems of fish-less tanks, tanks with a 60 μm mesh filter and tanks stocked at a fish density of 243 g m-3 were compared. In the presence of flathead grey mullets, cladocerans, ostracods and chironomid larvae became scarcer than in the control tanks, while there were more small phytoplankton and mud snails. The green algae Cladophorasp. did not occur at all. The presence of a mechanical filter also reduced cladoceran, ostracod and chironomid densities and increased phtyoplankton and mud snail density. However, the situation observed in filter tanks was intermediate between that observed in the fish tanks and the control tanks, due to the lower filtering efficiency of the mechanical filter. The organic matter content of the sediment decreased throughout the experiment in the control and filter tanks, but remained stable in fish tanks. Phosphorus and nitrogen concentrations were not affected by any treatment. These results showed that flathead grey mullet enhanced phytoplankton development due to the removal of large cladocerans and not as a consequence of nutrient release. Furthermore, the flathead grey mullet strongly modified the benthic community, probably due to direct predation.

Longer and Less Overlapping Food Webs in Anthropogenically Disturbed Marine Ecosystems: Confirmations from the Past

The human exploitation of marine resources is characterised by the preferential removal of the largest species. Although this is expected to modify the structure of food webs, we have a relatively poor understanding of the potential consequences of such alteration. Here, we take advantage of a collection of ancient consumer tissues, using stable isotope analysis and SIBER to assess changes in the structure of coastal marine food webs in the South-western Atlantic through the second half of the Holocene as a result of the sequential exploitation of marine resources by hunter-gatherers, western sealers and modern fishermen. Samples were collected from shell middens and museums. Shells of both modern and archaeological intertidal herbivorous molluscs were used to reconstruct changes in the stable isotopic baseline, while modern and archaeological bones of the South American sea lion Otaria flavescens, South American fur seal Arctocephalus australis and Magellanic penguin Spheniscus magellanicus were used to analyse changes in the structure of the community of top predators. We found that ancient food webs were shorter, more redundant and more overlapping than current ones, both in northern-central Patagonia and southern Patagonia. These surprising results may be best explained by the huge impact of western sealing on pinnipeds during the fur trade period, rather than the impact of fishing on fish populations. As a consequence, the populations of pinnipeds at the end of the sealing period were likely well below the ecosystems carrying capacity, which resulted in a release of intraspecific competition and a shift towards larger and higher trophic level prey. This in turn led to longer and less overlapping food webs.