Ten years after the Prestige Oil Spill: seabird trophic ecology as indicator of long-term effects on the coastal marine ecosystem

Major oil spills can have long-term impacts since oil pollution does not only result in acute mortality of marine organisms, but also affects productivity levels, predator-prey dynamics, and damages habitats that support marine communities. However, despite the conservation implications of oil accidents, the monitoring and assessment of its lasting impacts still remains a difficult and daunting task. Here, we used European shags to evaluate the overall, lasting effects of the Prestige oil spill (2002) on the affected marine ecosystem. Using δ15N and Hg analysis, we trace temporal changes in feeding ecology potentially related to alterations of the food web due to the spill. Using climatic and oceanic data, we also investigate the influence of North Atlantic Oscillation (NAO) index, the sea surface temperature (SST) and the chlorophyll a (Chl a) on the observed changes. Analysis of δ15N and Hg concentrations revealed that after the Prestige oil spill, shag chicks abruptly switched their trophic level from a diet based on a high percentage of demersal-benthic fish to a higher proportion of pelagic/semi-pelagic species. There was no evidence that Chl a, SST and NAO reflected any particular changes or severity in environmental conditions for any year or season that may explain the sudden change observed in trophic level. Thus, this study highlighted an impact on the marine food web for at least three years. Our results provide the best evidence to date of the long-term consequences of the Prestige oil spill. They also show how, regardless of wider oceanographic variability, lasting impacts on predator-prey dynamics can be assessed using biochemical markers. This is particularly useful if larger scale and longer term monitoring of all trophic levels is unfeasible due to limited funding or high ecosystem complexity

Using a three-isotope Bayesian mixing model to assess the contribution of refuse dumps in the diet of the yellow-legged gull Larus michahellis

SUMMARY.¿ The yellow-legged gull Larus michahellis is usually considered as an opportunistic species that depends on food derived from anthropogenic activity, such as garbage and fishery discards. However, although it has become a problematic species in many Mediterranean countries, there is stillno information about its status in Tunisia. The aim of this work was to assess the differential use of marine and terrestrial resources by the yellow-legged gulls breeding in an urban area on Chikly Island. Dietary reconstructions were performed through the analysis of regurgitates and δ13C, δ34S and δ15N of feathers of fledglings. Contrary to most Mediterranean breeding colonies, and to our expectations, the mixing model showed that yellow-legged gulls from Chikly are above all marine foragers. Whereas the Lake of Tunis was the principal source of food in 2005 and 2007, chicks from 2006 were fed mainly with prey from the Gulf of Tunis. Although the Gulf is located further from the breeding colony and has less fishing activity than the Lake, our study demonstrated that it is used as an alternative foraging habitat. The Bayesian mixing model approach proved to be a useful tool for evaluating temporal variations in the feeding ecology of the colony, which is relevant information in the management of a wild species. This study also demonstrated the importance of isotopic variability among years for inferring diet diversity and food availability for the colony, thereby allowing demographic forecasts when trophic resources vary in abundance or the foraging habitat is disturbed

High trophic niche overlap between a native and invasive mink does not drive trophic displacement of the native mink during an invasion process

The pressure elicited by invasive species on native species significantly increases with the increase of the overlap of their ecological niches. Still, the specific mechanisms of the trophic displacement of native species during the invasion process are unclear. The effects of the invasive American mink (Neovison vison) on the critically endangered European mink (Mustela lutreola) was assessed by analyses of diet and niche overlap during the invasion process. To do this, the isotopic composition (δ13C and δ15N) of both species of mink and their four main types of prey was analysed. Significant trophic overlap between the native European mink and invasive American mink was found when they coexisted in sympatry. Furthermore, both mink species were characterised by significant individual variation in diet and no obvious change in diet of the native species in response to the arrival of the introduced species was observed. High niche overlap registered between both species in sympatry with no displacement in diet of the native mink in response to the arrival of the invasive mink is expected to have important consequences for the viability and conservation of the native mink populations, as it suggests high competitive pressure

Stable isotopes and diet uncover trophic-niche divergence and ecological diversification processes of endemic reptiles on Socotra Island

Ecological diversification on islands typically results in divergence of ecological niches. As diet is a majorcomponent of species niches, we hypothesize that sister species within island monophyletic groupsdiversify in their dietary preferences. We have examined this hypothesis in two Haemodracon and fourHemidactylus species endemic reptiles of from Socotra Island (Yemen), corresponding to two indepen-dent colonization events. Convergence i.e., similar dietary patterns of phylogenetically unrelated species,was also examined. Trophic niches were studied by the analysis of carbon and nitrogen stable isotopescombined with faecal samples. We collected tail tips (for isotopes) and faecal pellets during two visitsin 2013 and 2014 to Socotra. Specific trophic niche widths inferred from stable isotopes were estimatedfrom ellipse-based metrics, whereas interspecific differences were compared by linear mixed models andexamined in a phylogenetic framework. From faecal samples, diet variation among species was quanti-fied by the Bray-Curtis index. Isotope and dietary interspecific divergence was compared with Manteltests. For both isotopes, models detected interspecific differences between sister species i.e., trophic nichedivergence and also interspecific similarities of distant lineages that use similar microhabitats i.e., ecolog-ical convergence. We did not find any phylogenetic signal neither in the interspecific differences in 13Cnor in 15N isotopic values; thus species phylogenetically more closely related did not have more similarisotopic niches. The Mantel test demonstrated similar interspecific divergence using isotopes and faecalsamples. In a phylogenetic context, trophic-niche interspecific comparisons highlight some mechanismsthat are driving ecological diversification and speciation of Socotra Island

Population control of an overabundant species achieved through consecutive anthropogenic perturbations

The control of overabundant vertebrates is often problematic. Much work has focused on population-level responses and overabundance due to anthropogenic subsidies. However, far less work has been directed at investigating responses following the removal of subsidies. We investigate the consequences of two consecutive perturbations-closure of a landfill and an inadvertent poisoning event- on the trophic ecology (13C, 15N and 34S), survival, and population size of an overabundant generalist seabird species, the yellow-legged gull. We expected that the landfill closure would cause a strong dietary shift and the inadvertent poisoning a decrease in gull population size. As a long-lived species, we also anticipated adult survival to be buffered against the decrease in food availability but not against the inadvertent poisoning event. Stable isotope analysis confirmed the dietary shift towards marine resources after the disappearance of the landfill. Although the survival model was inconclusive, it did suggest that the perturbations had a negative effect on survival, which was followed by a recovery back to average values. Food limitation likely triggered dispersal to other populations, while poisoning may have increased mortality; these two processes were likely responsible for the large fall in population size that occurred after the two consecutive perturbations. Life-history theory suggests that perturbations may encourage species to halt existing breeding investment in order to ensure future survival. However, under strong perturbation pulses the resilience threshold might be surpassed and changes in population density can arise. Consecutive perturbations may effectively manage overabundant species

Sex-specific foraging behaviour in response to fishing activities in a threatened seabird

Some seabird species have learnt to efficiently exploit fishing discards from trawling activities. However, a discard ban has been proposed as necessary in Europe to ensure the sustainability of the seas. It is of crucial importance for the management and conservation purposes to study the potential consequences of a discard ban on the foraging ecology of threatened seabirds. We assessed the influence of fishing activities on the feeding habits of 22 male and 15 female Audouin's gulls ( Larus audouinii ) from the Ebro Delta (Mediterranean Sea) during the breeding period using GPS loggers together with Stable Isotope Analysis (SIA), which provided new insights into their foraging behavior and trophic ecology, respectively. GPS data revealed different sex-specific foraging patterns between workdays and weekends. Females were highly consistent in that they foraged at sea throughout the week even though discarding stops at weekends. In contrast, males switched from foraging at sea during the week (when discards are produced) to an increased use of rice field habitats at week- ends (when fishermen do not work). This sex-specific foraging behavior could be related to specific nutritional requirements associated with previous egg pro- duction, an energetically demanding period for females. However, on a broader time scale integrated by the SIA, both sexes showed a high degree of individual specialization in their trophic ecology. The need to obtain detailed information on the dependence and response of seabirds to fishing activities is crucial in conservation sciences. In this regard, sex-specific foraging behavior in relation to fisheries has been overlooked, despite the ecological and conservation impli- cations. For instance, this situation may lead to sex differentiation in bycatch mortality in longlines when trawlers do not operate. Moreover, any new fisher- ies policy will need to be implemented gradually to facilitate the adaptation of a specialized species to a discard ban scenario

A physiological marker for quantifying differential reproductive investment between the sexes in Yellow-legged gulls (Larus michahellis)

Asymmetry between males and females in the energy they invest initially in reproduction has resulted in the evolution of differing reproductive strategies (caring females vs. competitive males). However, parental care in many birds is shared by both sexes suggesting that male energy expenditure in agonistic behaviors and courtship feeding might compensate female costs of clutch production. Here, we tested the hypothesis that initial investment in reproduction by both sexes in the Yellow-legged Gull (Larus michahellis), a species with biparental care, is similar from a physiological perspective. In this income breeder, female and male reproductive investment during early breeding can be ultimately related to muscular activity (local foraging effort required for clutch production in females and courtship feeding and agonistic behaviors in the case of males). Thus, we evaluated sex-specific patterns of creatine kinase (CK, IU/L) levels in plasma, an indicator of physical effort associated with muscular activity dependent behaviors, through incubation as a reflection of the physiological response of both sexes to the reproductive investment they made up to clutch completion. Raw levels of CK were related to plasma levels of total proteins (TP, g/dL) to account for the differential physiological state of individuals when sampled (i.e. differential dehydratation). Female costs of clutch production were associated with post-laying levels of CK/TP. We grouped females according to their relative investment in clutch production: 17.3% of field metabolic rate; which showed increasing values of CK/TP (24.6, 53.1 and 66.0 IU/g, respectively). Moreover, we found similar CK/TP trends throughout incubation for both sexes (CK/TP = 50.2- [3.3 x days from laying]) suggesting similar physiological responses to reproductive effort and, therefore, analogous sex-specific initial investment. Thus, male investment in agonistic behaviors and courtship feeding apparently equaled female investment in clutch production. The use of CK measurements is revealed as a useful approach to investigating overall investment in reproduction for both sexes, providing further insights into our comprehension of reproductive strategies in seabirds

Modelling terrestrial and marine foraging habitats in breeding Audouin's gulls Larus audouinii: timing matters

Although the breeding ecology of Audouin's gull has been widely studied, its spatial distribution patterns have received little attention. We assessed the foraging movements of 36 GPS-tracked adult Audouin's gulls breeding at the Ebro Delta (NW Mediterranean), coinciding with the incubation period (May 2011). This also coincided with a trawling moratorium northwards from the colony. We modelled the distribution of the gulls by combining these tracking data with environmental variables (including fishing activities from Vessel Monitoring System, VMS), using Maxent. The modelling range included both marine and terrestrial areas. Models were produced separately for every 2h time interval across the day, and for 2 fishing activity scenarios (workdays vs. weekends), allowing to assess the spatio-temporal distribution patterns of the gulls and the degree of association with fisheries. During workdays, gull distribution at sea fully matched with fishing activities, both trawling (daylight) and purse-seining (nightime). Gulls tended to avoid the area under trawling moratorium, confirming the high influence of fisheries on the distribution patterns of this species. On weekends, gulls made lesser use of the sea and tended to increase the use of rice fields. Overall, Audouin's gull activity was more intense during dailight hours, although birds also showed nocturnal activity, on both workdays and weekends. Nocturnal patterns at sea were more disperse during the latter, probably because these gulls are able to capture small pelagic fish at night in natural conditions, but tend to congregate around purse-seiners (which would enhance their foraging efficiency) in workdays. These results provide important insight for the management of this species. This is of particular relevance under the current scenario of European fisheries policies, since new regulations are aimed at eliminating discards, and this would likely influence Audouin's gull populations

Metals and Selenium as bioindicators of geographic and trophic segregation in Giant Petrels Macronectes spp.

We analysed concentrations of cadmium, lead, mercury and selenium in blood from males and females of the 2 sibling species of giant petrels, the northern Macronectes halli and the southern M. giganteus, breeding sympatrically at Bird Island (South Georgia, Antarctica). Blood samples were collected in 1998 during the incubation period, from 5 November to 10 December. Between species, cadmium and lead concentrations were significantly higher for northern than for southern giant petrels, which probably resulted from northern giant petrels wintering in more polluted areas (mainly on the Patagonian Shelf and Falkland Islands) compared to southern giant petrels (wintering mainly around South Georgia and the South Sandwich Islands). Between sexes, cadmium concentrations were significantly higher for females than for males in both species, corresponding to the more pelagic habits of females compared to the more scavenging habits of males. Lead and cadmium concentrations in circulating blood decreased significantly over the incubation period, suggesting that when breeding at Bird Island, exposure to the source of pollution had ended, and these metals had been cleared from the blood and excreted, or rapidly transferred to other tissues. Association of lead and cadmium with a common source of pollution was further corroborated by a significant positive correlation between the levels of the 2 elements found. Mercury levels were similar between the species, but showed an opposite trend between sexes, with males showing higher levels than females in northern giant petrels, and the opposite was true in southern giant petrels, with no changes throughout incubation. Selenium levels were similar between sexes, but significantly greater for northern than for southern giant petrels. Moreover, there was a significant increase in the selenium levels over the incubation period in northern giant petrels. Age of adult birds did not affect metal concentrations. Coefficients of variation of metal levels were consistently lower for northern than for southern giant petrels, particularly for mercury, suggesting that the former species is more dietary specialised than the latter. Contaminant analyses, when combined with accurate information on seabird movements, obtained through geolocation or satellite tracking, help us to understand geographic variation of pollution in the marine environment

Telomere shortening rate predicts species life span

Telomere shortening to a critical length can trigger aging and shorter life spans in mice and humans by a mechanism that involves induction of a persistent DNA damage response at chromosome ends and loss of cellular viability. However, whether telomere length is a universal determinant of species longevity is not known. To determine whether telomere shortening can be a single parameter to predict species longevities, here we measured in parallel the telomere length of a wide variety of species (birds and mammals) with very different life spans and body sizes, including mouse (Mus musculus), goat (Capra hircus), Audouin's gull (Larus audouinii), reindeer (Rangifer tarandus), griffon vulture (Gyps fulvus), bottlenose dolphin (Tursiops truncatus), American flamingo (Phoenicopterus ruber), and Sumatran elephant (Elephas maximus sumatranus). We found that the telomere shortening rate, but not the initial telomere length alone, is a powerful predictor of species life span. These results support the notion that critical telomere shortening and the consequent onset of telomeric DNA damage and cellular senescence are a general determinant of species life span