Leatherback turtles as oceanographic indicators: stable isotope analyses reveal a trophic dichotomy between ocean basins

Oceanographic sampling is often limited to local and temporally concise assessments of complex, transient, and widespread phenomena. However, long-lived, migratory pelagic vertebrates such as leatherback turtles (Dermochelys coriacea, Vandelli 1761) can provide important integrated information about broad-scale oceanographic processes. Therefore, the present study analyzed stable carbon and nitrogen isotope ratios (δ¹³C and δ¹⁵N) of egg yolk and red blood cells from nesting leatherback populations from Costa Rica in the eastern Pacific in 2003–2004 and 2004–2005 and from St. Croix in the North Atlantic in 2004 and 2005 to establish differences between nutrient sourcing and its influence on higher trophic level consumers in both ocean basins. Whereas δ¹³C signatures were similar between Costa Rica (−19.1±0.7‰) and St. Croix (−19.4±1.0‰) leatherbacks, reflecting the pelagic foraging strategy of the species, Costa Rica leatherback δ¹⁵N signatures (15.4±1.8‰) were significantly enriched relative to St. Croix leatherback δ¹⁵N signatures (9.8±1.5‰). This δ¹⁵N difference likely reflects inter-basin differences in nitrogen cycling regimes and their influence on primary productivity being transferred through several trophic levels. Thus, high-order marine consumer movements, habitat preferences, and stable isotope signatures can be combined with ocean sampling to elucidate interactions between oceanographic processes and marine megafauna.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Biological and environmental influences on the trophic ecology of leatherback turtles in the northwest Atlantic Ocean

Understanding the causes and consequences of variability in trophic status is important for interpreting population dynamics and for identifying important habitats for protected species like marine turtles. In the northwest Atlantic Ocean, many leatherback turtles (Dermochelys coriacea) from distinct breeding stocks throughout the Wider Caribbean region migrate to Canadian waters seasonally to feed, but their trophic status during the migratory and breeding cycle and its implications have not yet been described. In this study, we used stable carbon and nitrogen isotope analyses of bulk skin to characterize the trophic status of leatherbacks in Atlantic Canadian waters by identifying trophic patterns among turtles and the factors influencing those patterns. δ¹⁵N values of adult males and females were significantly higher than those of turtles of unknown gender (i.e., presumed to be subadults), and δ¹⁵N increased significantly with body size. We found no significant differences among average stable isotope values of turtles according to breeding stock origin. Significant inter-annual variation in δ¹⁵N among cohorts probably reflects broad-scale oceanographic variability that drives fluctuations in stable isotope values of nutrient sources transferred through several trophic positions to leatherbacks, variation in baseline isotope values among different overwintering habitats used by leatherbacks, or a combination of both. Our results demonstrate that understanding effects of demographic and physiological factors, as well as oceanographic conditions, on trophic status is key to explaining observed patterns in population dynamics and for identifying important habitats for widely distributed, long-lived species like leatherbacks.     

Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions

Interactions with fisheries are believed to be a major cause of mortality for adult leatherback turtles (Dermochelys coriacea), which is of particular concern in the Pacific Ocean, where they have been rapidly declining. In order to identify where these interactions are occurring and how they may be reduced, it is essential first to understand the movements and behavior of leatherback turtles. There are two regional nesting populations in the East Pacific (EP) and West Pacific (WP), comprising multiple nesting sites. We synthesized tracking data from the two populations and compared their movement patterns. A switching state-space model was applied to 135 Argos satellite tracks to account for observation error, and to distinguish between migratory and area-restricted search behaviors. The tracking data, from the largest leatherback data set ever assembled, indicated that there was a high degree of spatial segregation between EP and WP leatherbacks. Area-restricted search behavior mainly occurred in the southeast Pacific for the EP leatherbacks, whereas the WP leatherbacks had several different search areas in the California Current, central North Pacific, South China Sea, off eastern Indonesia, and off southeastern Australia. We also extracted remotely sensed oceanographic data and applied a generalized linear mixed model to determine if leatherbacks exhibited different behavior in relation to environmental variables. For the WP population, the probability of area-restricted search behavior was positively correlated with chlorophyll-a concentration. This response was less strong in the EP population, but these turtles had a higher probability of search behavior where there was greater Ekman upwelling, which may increase the transport of nutrients and consequently prey availability. These divergent responses to oceanographic conditions have implications for leatherback vulnerability to fisheries interactions and to the effects of climate change. The occurrence of leatherback turtles within both coastal and pelagic areas means they have a high risk of exposure to many different fisheries, which may be very distant from their nesting sites. The EP leatherbacks have more limited foraging grounds than the WP leatherbacks, which could make them more susceptible to any temperature or prey changes that occur in response to climate change.     

Temporal and spatial variation in the δ<Superscript>15</Superscript>N and δ<Superscript>13</Superscript>C values of fish and squid from Alaskan waters

To test the hypothesis that stable isotope ratios from marine organisms vary, the δ¹⁵N and δ¹³C values from fish and squid collected in Alaskan waters were measured across years (1997, 2000, and 2005), seasons, geographic locations, and different size/age classes, and between muscle tissue and whole animals. Temporal, geographic, and ontogenetic differences in stable isotope ratios ranged from 0.5–2.5‰ (δ¹⁵N) to 0.5–2.0‰ (δ¹³C). Twenty-one comparisons of stable isotope values between whole organisms and muscle tissue revealed only four small differences each for δ¹⁵N and δ¹³C, making costly and space prohibitive collection of whole animals unnecessary. The data from this study indicate that significant variations of stable isotope values from animals in marine systems necessitates collection of prey and predator tissues from the same time and place for best interpretation of stable isotope analysis in foraging ecology studies.     

Central place foraging by breeding Cook’s petrel Pterodroma cookii: foraging duration reflects range, diet and chick meal mass

Pelagic seabirds are central place foragers during breeding and variation in foraging trip duration and range reflect differences in diet and chick provisioning, through the exploitation of divergent habitats of varying productivity. We tested whether these relationships hold in small procellarriids by equipping chick-rearing Cook’s petrel Pterodroma cookii (200 g) with geolocation-immersion loggers, conducting isotope analysis of blood and measuring chick meal mass following foraging trips of varying duration. Cook’s petrel tracked during chick rearing from Little Barrier Island (LBI) and Codfish Island (CDF), New Zealand had larger maximum ranges during longer foraging trips. Blood nitrogen isotope signatures (δ¹⁵N) of adults were significantly higher after foraging trips of longer duration, but not of greater maximum range. There was no significant relationship between blood carbon isotope signatures (δ¹³C) and foraging trip characteristics. Proportion of time spent on the sea surface and the mass of the meal brought back to chicks were consistently greater for Cook’s petrel with larger maximum ranges, which in the case of birds from CDF coincided with productive subtropical convergence zone habitats. As predicted, trip duration reflected divergent foraging behaviours in Cook’s petrel during breeding. We suggest that the availability of different prey is a key factor governing at-sea distributions and dietary composition of this species.     

Stable isotopes identify age- and sex-specific dietary partitioning and foraging habitat segregation in southern giant petrels breeding in Antarctica and southern Patagonia

We examined the isotopic signatures (δ¹³C, δ¹⁵N) of adult body feathers from southern giant petrels Macronectes giganteus collected at two breeding colonies in Antarctica (Potter Peninsula and Cape Geddes) and one in southern Patagonia (Observatorio Island), as well as in whole blood collected from adults of both sexes at each Antarctic colonies and from chicks at Potter Peninsula. As body feather moult is a continuous process in giant petrels, feathers provide an integrated annual signal of an adult’s diets and foraging habitats. In contrast, the stable isotope values of adult and chick blood are reflective of their diets during the breeding season. We found that sex-specific dietary segregation in adults breeding in Antarctica was notable during the breeding season (blood samples) but absent when examined across the entire year (feather samples). In addition, blood stable isotope values differed between chicks and adults, indicating that adults provision their offspring with a relatively higher amount of penguin and seal prey that what they consume themselves. This finding confirms previous work that suggests that chicks are preferentially fed with prey of presumably higher nutritional value such as carrion. Finally, based on isotopic differences between major oceanographic zones in the Southern Ocean, our data indicate population-specific differences in foraging distribution, with Antarctic populations move seasonally between Antarctic and subantarctic zones, while Patagonian populations likely forage in subtropical waters and in continental shelf habitats year-round.     

A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii

Within the tropical and subtropical oceans, tuna forage opportunistically on a wide variety of prey. However, little is known about the trophic ecology of the smallest size classes which play an important role in stock assessments and fisheries management. The foraging behavior of yellowfin tuna, Thunnus albacares (23.5–154.0 cm FL), collected from nearshore Fish Aggregating Devices (FADs) around Oahu was studied using stable isotope and stomach contents analyses. Emphasis was placed on small juveniles. Yellowfin tuna changed their diets significantly between 45 and 50 cm forklength (ca. 1.5 kg). Smallest size classes fed on planktonic organisms inhabiting the shallow mixed layer, primarily larval stomatopod and decapod crustaceans, whereas larger tuna fed on teleosts and adult Oplophorus gracilirostris, a vertically migrating mesopelagic species of shrimp. When interpreting the variation in prey δ ¹⁵N values, we considered both their relative trophic position and δ ¹⁵N values of the nitrogen at the base of the food web. Based on the distinct diet shift of the yellowfin tuna, demonstrated by both isotope and stomach content analyses, we propose a critical mass threshold was reached at about 45 cm FL that enabled sufficient endothermic capability to allow tuna to access prey dwelling in deeper, colder water. These ontogenetic changes in foraging range and commensurate shift in diet of small tunas would affect their vulnerability to fishing pressure.     

Comparative foraging ecology and ecological niche of a superabundant tropical seabird: the sooty tern Sterna fuscata in the southwest Indian Ocean

Over 6-million pairs of sooty terns Sterna fuscata breed once a year in the southwest Indian Ocean, mostly on three islands of the Mozambique Channel (Europa, Juan de Nova and Glorieuses) and in the Seychelles region. Seasonal reproduction in either winter or summer is the dominant strategy in the area, but non-seasonal reproduction also occurred in some places like at Glorieuses Archipelago. The feeding ecology of the sooty tern was investigated during the breeding seasons to determine whether terns showed significant differences in their trophic ecology between locations. Regurgitations were analyzed to describe the diet of individuals when breeding, and stable isotopes and mercury concentrations were used to temporally integrate over the medium-term of the trophic ecology of both adults and chicks. Overall, the diet was composed of fish, flying squid and fish larvae in different proportions. At Europa and Aride in the Seychelles, where winter reproduction occurs, large epipelagic prey like flying fish or squid dominated the diet. At Juan de Nova, sooty terns reproduce in summer and rely mostly on fish larvae. At Glorieuses (non-seasonal breeding), the diet was intermediate with fish larvae and flying squid being important prey items. The stable-carbon and nitrogen isotope values in blood confirm the differences observed in dietary analysis, and demonstrate different feeding strategies between colonies. δ¹³C values of feathers showed spatial segregation between birds from the Mozambique Channel and the Seychelles region. Terns from the Seychelles had also higher δ¹⁵N values. Feather δ¹³C values also suggest a significant shift from summer to wintering habitat for birds from Juan de Nova. This study emphasizes the high phenotypic plasticity of the species, which may explain its numerical dominance in all tropical waters of the World’s Ocean.     

A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain

The widespread omnivory of consumers and the trophic complexity of marine ecosystems make it difficult to infer the feeding ecology of species. The use of stable isotopic analysis plays a crucial role in elucidating trophic interactions. Here we analysed δ¹⁵N, δ¹³C and δ³⁴S in chick feathers, and we used a Bayesian triple-isotope mixing model to reconstruct the diet of a generalist predator, the yellow-legged gull (Larus michahellis) that breeds in the coastal upwelling area off northwest mainland Spain. The mixing model indicated that although chicks from all colonies were fed with a high percentage of fish, there are geographical differences in their diets. While chicks from northern colonies consume higher percentages of earthworms, refuse constitutes a more important source in the diet of chicks from western colonies. The three-isotope mixing model revealed a heterogeneity in foraging habitats that would not have been apparent if only two stable isotopes had been analysed. Moreover, our work highlights the potential of adding δ³⁴S for distinguishing not only between terrestrial and marine prey, but also between different marine species such as fish, crabs and mussels.     

Delayed ontogenic dietary shift and high levels of omnivory in green turtles (<Emphasis Type="Italic">Chelonia mydas</Emphasis>) from the NW coast of Africa

Young green turtles (Chelonia mydas) spend their early lives as oceanic omnivores with a prevalence of animal prey. Once they settle into neritic habitats (recruitment), they are thought to shift rapidly to an herbivorous diet, as revealed by studies in the Greater Caribbean. However, the precise timing of the ontogenic dietary shift and the actual relevance of animal prey in the diet of neritic green turtles are poorly known elsewhere. Stable isotopes of carbon, sulfur and nitrogen in the carapace scutes of 19 green turtles from Mauritania (NW Africa), ranging from 26 to 102 cm in curved carapace length (CCLmin), were analyzed to test the hypothesis of a rapid dietary shift after recruitment. Although the length of residence time in neritic habitats increased with turtle length, as revealed by a significant correlation between turtle length and the δ¹³C and the δ³⁴S of the scutes, comparison of the δ¹⁵N of the innermost and outermost layers of carapace scutes demonstrated that consumption of macrophytes did not always start immediately after recruitment, and turtles often resumed an animal-based diet after starting to graze on seagrasses. As a consequence, seagrass consumption did not increase gradually with turtle size and animal prey largely contributed to the diet of turtles within the range 29–59 cm CCLmin (76–99% of assimilated nutrients). Seagrass consumption by turtles larger than 59 cm CCLmin was higher, but they still relied largely on animal prey (53–76% of assimilated nutrients). Thus, throughout most of their neritic juvenile life, green turtles from NW Africa would be better classified as omnivores rather than herbivores. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki

Sea lions are generally considered opportunistic feeders. However, studies from different areas suggest their diet consists mostly of four to five types of prey. Previous studies in Galapagos sea lions have identified at least three feeding strategies for this species, suggesting diversification of their diet. Diet diversification is favored in organisms with relatively high trophic position and subject to high intra-specific and low inter-specific competition. Zalophus wollebaeki meet these criteria as the only pinniped on San Cristobal Island, where three sea lion rookeries are located within 11 km: a distance considerably shorter than their 41 km foraging range. To measure the degree of diet diversification, we used scats and stable isotope analyses. A total of 270 scat samples from lactating females and 142 fur samples from sea lion pups were collected during the breeding season 2006. The scat analysis identified distinct diets among rookeries, with minimal trophic overlap (Cλ = 0.19), a trophic level TL = 4.5 (secondary–tertiary carnivore), and trophic breadth of a specialist predator (B _i  = 0.37). The mean δ¹⁵N and δ¹³C values were 13.07 ± 0.52 and −16.34 ± 0.37, respectively. No significant difference was found in the δ¹⁵N values from the sea lion rookeries, but differences were found inter- and intra-population in δ¹³C values for pups from different groups (ANOVA P < 0.05). Our results indicate that diet diversification is present in the Galapagos sea lion and may play important role to the survival of the species in a habitat where pinniped populations are limited.     

Polymodal foraging in adult female loggerheads (Caretta caretta)

To determine whether loggerhead turtles (Caretta caretta) nesting in southeastern USA exhibit polymorphic foraging strategies, we evaluated skin samples for stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) from 310 loggerheads from four locations on the east coast of Florida and epibionts from 48 loggerheads. We found a dichotomy between a depleted δ¹³C cluster and an enriched δ¹³C cluster. Epibionts from oceanic/pelagic or neritic/benthic habitats were largely consistent with this dichotomy. The bimodal distribution of δ¹³C could reflect a bimodal foraging strategy or—because of the potential for confounding among four gradients of δ¹³C in marine environments—a polymodal foraging strategy. We integrate our results with results from other stable isotope studies, satellite telemetry, and flipper tags to evaluate potential foraging strategies. Understanding foraging strategies is essential for development of management plans for this endangered species that has suffered a 43% population decline over the last decade.     

Bottom-up and climatic forcing on the worldwide population of leatherback turtles

Nesting populations of leatherback turtles (Dermochelys coriacea) in the Atlantic and western Indian Oceans are increasing or stable while those in the Pacific are declining. It has been suggested that leatherbacks in the eastern Pacific may be resource limited due to environmental variability derived from the El Ni?o Southern Oscillation (ENSO), but this has yet to be tested. Here we explored bottom-up forcing and the responding reproductive output of nesting leatherbacks worldwide. We achieved this through an extensive review of leatherback nesting and migration data and by analyzing the spatial, temporal, and quantitative nature of resources as indicated by net primary production at post-nesting female migration and foraging areas. Leatherbacks in the eastern Pacific were the smallest in body size and had the lowest reproductive output due to less productive and inconsistent resources within their migration and foraging areas. This derived from natural interannual and multidecadal climate variability together with an influence of anthropogenic climate warming that is possibly affecting these natural cycles. The reproductive output of leatherbacks in the Atlantic and western Indian Oceans was nearly twice that of turtles in the eastern Pacific. The inconsistent nature of the Pacific Ocean may also render western Pacific leatherbacks susceptible to a more variable reproductive output; however, it appears that egg harvesting on nesting beaches is their major threat. We suggest that the eastern Pacific leatherback population is more sensitive to anthropogenic mortality due to recruitment rates that are lower and more variable, thus accounting for much of the population differences compared to Atlantic and western Indian turtles.     

Use of multiple tools to assess the feeding preference of coastal dolphins

The feeding preferences of the coastal dolphins Pontoporia blainvillei and Sotalia guianensis in south-eastern Brazil (21o18′S–22o25′S) were assessed through the prey’s index of relative importance (IRI), total mercury concentration (Hg_tot), and stable isotopic (δ¹⁵N and δ¹³C) to compare their efficiency in the discrimination of prey contribution to the predators’ diet. The IRI was the best tool to describe the dolphins’ preference, while Hg_tot and δ¹⁵N seemed to be efficient as a trophic marker when the diet is made up of prey of varying sizes, as observed in S. guianensis. Both dolphins presented lighter δ¹⁵N than their prey species, which is an unusual pattern. However, as the sample size to isotope ratios analysis was small, especially to the dolphins, the results should be considered with caution, and further studies are necessary to corroborate these findings. The δ¹³C values characterized a typical coastal food chain, confirming the preferential area of these species.     

Variability of albacore (<Emphasis Type="Italic">Thunnus alalunga</Emphasis>) diet in the Northeast Atlantic and Mediterranean Sea

This study aims to describe the variability of albacore (Thunnus alalunga) diet in the Northeast Atlantic and Mediterranean Sea and to identify possible relationships between this variability and the features of different feeding areas, the behavior, and the energetic needs of albacore. Stomach contents from albacore caught in five zones of the Bay of Biscay and surrounding waters (n = 654) and three zones of the Mediterranean Sea (n = 152) were analyzed in terms of diet composition and stomach fullness. Carbon and nitrogen stable isotope and C/N ratios were measured for white muscle and liver from albacore in the Bay of Biscay (n = 41) and Mediterranean Sea (n = 60). Our results showed a spatial, seasonal, inter-annual, and size-related variability in the diet of albacore. Albacore diet varied by location in the Mediterranean Sea, with a particularly high proportion of cephalopods, and low δ¹⁵N values in the Tyrrhenian Sea. In the Northeast Atlantic, albacore consumed a higher proportion of crustaceans and a lower proportion of fishes in the most offshore sampling zone than inshore. The digestion states of the major prey reflected a diurnal feeding activity, indicative of feeding in deeper waters offshore, whereas on the continental slope, feeding probably occurred in surface waters at night. Important seasonal and inter-annual diet variability was observed in the southeast of the Bay of Biscay, where preferred albacore prey appeared to be anchovy (Engraulis encrasicolus). Stomach fullness was inversely related to body size, probably reflecting higher energetic needs for smaller individuals. Albacore from the Bay of Biscay had significantly lower δ¹³C and higher δ¹⁵N values compared with albacore from the Mediterranean Sea, indicative of regional baseline shifts, and trophic position and muscle lipid stores in albacore increased with body size.     

Distribution of foraging habitats of male loggerhead turtles (Caretta caretta) as revealed by stable isotopes and satellite telemetry

Most studies on the foraging ecology of loggerhead turtles (Caretta caretta) have focused on adult females and juveniles. Little is known about the foraging patterns of adult male loggerheads. We analyzed tissues for carbon and nitrogen stable isotopes (δ¹³C and δ¹⁵N) from 29 adult male loggerheads tracked with satellite transmitters from one breeding area in Florida, USA, to evaluate their foraging habitats in the Northwest Atlantic (NWA). Our study revealed large variations in δ¹³C and δ¹⁵N and a correlation between both δ¹³C and δ¹⁵N and the latitude to which the loggerheads traveled after the mating season, thus reflecting a geographic pattern in the isotopic signatures. Variation in δ¹³C and δ¹⁵N can be explained by differences in food web baseline isotopic signatures rather than differences in loggerhead trophic levels. Stable isotope analysis may help elucidate residency and migration patterns and identify foraging sea turtle subpopulations in the NWA due to the isotopically distinct habitats used by these highly migratory organisms.     

Diet of the social groups of long-finned pilot whales (<Emphasis Type="Italic">Globicephala melas</Emphasis>) in the Strait of Gibraltar

The Strait of Gibraltar is inhabited throughout the year by a group of pilot whales (Globicephala melas), but their spatial distribution varies between Summer and Autumn. In this paper, we have used carbon (¹³C/¹²C) and nitrogen (¹⁵N/¹⁴N) stable isotope signatures to investigate the differences in diet amongst seasons, sex and stable social units. Skin samples were collected from 56 individually photo-identified pilot whales during Autumn 2005 and Summer 2006. These individuals were genetically sexed and their isotopic signature determined. The level of inter-individual association both within and between stable social units were compared to Euclidean distances between individual isotopes signatures. No differences in either δ¹⁵N or δ¹³C were found according to the sex of individuals, but significant seasonal differences were found in δ¹⁵N, although not in the δ¹³C values. This suggests that pilot whales are resident year round in the Strait, a finding supported by independent photo-identification. The variation in δ¹⁵N could reflect a shift in pilot whale diet through the year, with pilot whales feeding at a higher trophic level in Autumn compared to Summer. This could also represent a change in the diet of pilot whale prey species. The δ¹³C values were significantly different amongst the four stable social units sampled and individual δ¹³C values were significantly related to the level of inter-individual association, while no relationship was found for δ¹⁵N. These results suggest that within the same general area (i.e. the Strait of Gibraltar), there is some level of specialisation in habitat or prey choice between pilot whales social units.     

Spatio-temporal variations in the diet and stable isotope composition of the Argentine hake <Emphasis Type="Italic">Merluccius hubbsi</Emphasis> Marini, 1933 of the continental shelf of southeastern Brazil

The feeding ecology of Merluccius hubbsi was investigated in 2 regions of SE Brazil. The major food sources for the hakes were fish, crustaceans, and squid. In the upwelling system of Cabo Frio, the diet was very similar in the summers of 2001/2002 and spring 2002; fish were the most important prey followed by crustaceans. In Ubatuba, euphausiids were an important prey during the winter 2001 (100 m), while in the summer 2002, fish and amphipods predominated in the diet in the shallower site (40 m) and squid in the deeper site (100 m). The hakes showed temporal differences in stable isotope signatures in both regions, while C:N ratios varied only in Cabo Frio. δ¹⁵N and δ¹³C (bulk and corrected for lipid content) increased with fish length, which seems to be related to the increasing importance of fish and decreasing importance of euphausiids and amphipods in the diet of larger hakes. The mean trophic level of 3.7 for M. hubbsi was estimated using δ¹⁵N of bivalves as baseline and the fractionation of 3.4‰ between trophic levels.     

Feeding ecology of the grooved tiger shrimp <Emphasis Type="Italic">Penaeus semisulcatus</Emphasis> De Haan (Decapoda: Penaeidae) in inshore waters of Qatar,Arabian Gulf

The feeding ecology of the green tiger shrimp Penaeus semisulcatus was studied in inshore fishing grounds off Doha, Qatar, using a combination of stable isotope (δ¹³C and δ¹⁵N) analysis and gut contents examination. Samples of post-larvae, juvenile and adult shrimp and other organisms were collected from intertidal and subtidal zones during the spawning season (January–June). Shrimp collected from shallow water seagrass beds were mostly post-larvae and juveniles and were significantly smaller than the older juveniles and adults caught in deeper macroalgal beds. Gut content examination indicated that post-larvae and juvenile shrimp in seagrass beds fed mainly on benthos such as Foraminifera, polychaetes, benthic diatoms and small benthic crustaceans (amphipods, isopods and ostracoda), whereas larger shrimp in the macroalgal beds fed mainly on bivalve molluscs and to a lesser extent polychaetes. In shrimp from both seagrass and algal beds, unidentifiable detritus was also present in the gut (18, 32%). δ¹³C values for shrimp muscle tissue ranged from −9.5 ± 0.26 to −12.7 ± 0.05‰, and δ¹⁵N values increased with increasing shrimp size, ranging from 4.1 ± 0.03 to 7.7 ± 0.11‰. Both δ¹⁵N values and δ¹³C values for shrimp tissue were consistent with the dietary sources indicated by gut contents and the δ¹³C and δ¹⁵N values for primary producers and prey species. The combination of gut content and stable isotope data demonstrates that seagrass beds are important habitats for post-larvae and juvenile P. semisulcatus, while the transition to deeper water habitats in older shrimp involves a change in diet and source of carbon and nitrogen that is reflected in shrimp tissue stable isotope ratios. The results of the study confirm the linkage between sensitive shallow water habitats and the key life stages of an important commercially-exploited species and indicate the need for suitable assessment of the potential indirect impacts of coastal developments involving dredging and land reclamation.     

Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards

Pelagic seabirds obtain food from oceans where the availability of their prey changes rapidly both seasonally and spatially. Here, we investigated changes in the trophic habits of the critically endangered Balearic shearwater (Puffinus mauretanicus) through the breeding season and tested for dietary differences between sexes and age classes. We analysed δ¹⁵N and δ¹³C values in blood of adults during the pre-incubation, incubation and chick-rearing periods and of their chicks. Using a two-isotope mixing model, we estimated dietary contributions based on isotope values from potential prey species which included small pelagic species available naturally and demersal fish species available only from trawling discards. Balearic shearwaters showed clear isotopic and dietary variation through the breeding season. During pre-incubation, breeding adults appeared to exploit demersal fish, whereas during the incubation and chick-rearing period, they fed mainly on pelagic anchovies (Engraulis encrasicolus) and pilchards (Sardina pilchardus). Similarly, chicks were fed mainly with anchovies, a resource with a high energetic value. This variation in the dietary habits of adult shearwaters during the breeding season was probably related to both natural and fishery-induced seasonal changes in the availability of potential prey species within their main feeding grounds. However, changes in the nutritional requirements of the shearwaters could also play an important role. Indeed, diet differed between sexes during pre-incubation: females fed less on trawling discards and more on small pelagic fish than males. This sexual segregation in diet could be the consequence of higher nutritional requirements of females during this period. Our study reveals the differential importance of both trawling discards and small pelagic fish species for a pelagic seabird depending on the breeding period and illustrates the importance of considering the entire breeding season when making inferences about the importance of specific prey in seabird dietary studies.