Parenting in a warming world: thermoregulatory responses to heat stress in an endangered seabird.

The frequency of extreme weather events, including heat waves, is increasing with climate change. The thermoregulatory demands resulting from hotter weather can have catastrophic impacts on animals, leading to mass mortalities. Although less dramatic, animals also experience physiological costs below, but approaching, critical temperature thresholds. These costs may be particularly constraining during reproduction, when parents must balance thermoregulation against breeding activities. Such challenges should be acute among seabirds, which often nest in locations exposed to high solar radiation and predation risk. The globally endangered bank cormorant Phalacrocorax neglectus breeds in southern Africa in the winter, giving little scope for poleward or phenological shifts in the face of increasing temperatures. Physiological studies of endangered species sensitive to human disturbance, like the bank cormorant, are challenging, because individuals cannot be captured for experimental research. Using a novel, non-invasive, videographic approach, we investigated the thermoregulatory responses of this seabird across a range of environmental temperatures at three nesting colonies. The time birds spent gular fluttering, a behaviour enhancing evaporative heat loss, increased with temperature. Crouching or standing birds spent considerably less time gular fluttering than birds sitting on nests (ca 30% less at 22°C), showing that postural adjustments mediate exposure to heat stress and enhance water conservation. Crouching or standing, however, increases the vulnerability of eggs and chicks to suboptimal temperatures and/or expose nest contents to predation, suggesting that parents may trade-off thermoregulatory demands against offspring survival. We modelled thermoregulatory responses under future climate scenarios and found that nest-bound bank cormorants will gular flutter almost continuously for several hours a day by 2100. The associated increase in water loss may lead to dehydration, forcing birds to prioritize survival over breeding, a trade-off that would ultimately deteriorate the conservation status of this species.

A non-invasive approach to estimate the energetic requirements of an increasing seabird population in a perturbed marine ecosystem.

There is a growing desire to integrate the food requirements of predators living in marine ecosystems impacted by humans into sustainable fisheries management. We used non-invasive video-recording, photography and focal observations to build time-energy budget models and to directly estimate the fish mass delivered to chicks by adult greater crested terns Thalasseus bergii breeding in the Benguela ecosystem. Mean modelled adult daily food intake increased from 140.9 g·d-1 of anchovy Engraulis capensis during incubation to 171.7 g·d-1 and 189.2 g·d-1 when provisioning small and large chicks, respectively. Modelled prey intake expected to be returned to chicks was 58.3 g·d-1 (95% credible intervals: 44.9-75.8 g·d-1) over the entire growth period. Based on our observations, chicks were fed 19.9 g·d-1 (17.2-23.0 g·d-1) to 45.1 g·d-1 (34.6-58.7 g·d-1) of anchovy during early and late provisioning, respectively. Greater crested terns have lower energetic requirements at the individual (range: 15-34%) and population level (range: 1-7%) than the other Benguela endemic seabirds that feed on forage fish. These modest requirements - based on a small body size and low flight costs - coupled with foraging plasticity have allowed greater crested terns to cope with changing prey availability, unlike the other seabirds species using the same exploited prey base.

Foraging plasticity in seabirds: A non-invasive study of the diet of greater crested terns breeding in the Benguela region.

Marine predators, such as seabirds, are useful indicators of marine ecosystem functioning. In particular, seabird diet may reflect variability in food-web composition due to natural or human-induced environmental change. Diet monitoring programmes, which sample diet non-invasively, are valuable aids to conservation and management decision-making. We investigated the diet of an increasing population of greater crested terns Thalasseus bergii in the Western Cape, South Africa, during three successive breeding seasons (2013 to 2015), when populations of other seabirds feeding on small pelagic schooling fish in the region were decreasing. Breeding greater crested terns carry prey in their bills, so we used an intensive photo-sampling method to record their diet with little disturbance. We identified 24,607 prey items from at least 47 different families, with 34 new prey species recorded. Fish dominated the diet, constituting 94% of prey by number, followed by cephalopods (3%), crustaceans (2%) and insects (1%). The terns mainly targeted surface-schooling Clupeiformes, with anchovy Engraulis encrasicolus the most abundant prey in all three breeding seasons (65% overall). Prey composition differed significantly between breeding stages and years, with anchovy most abundant at the start of the breeding season, becoming less frequent as the season progressed. The proportion of anchovy in the diet also was influenced by environmental factors; anchovy occurred more frequently with increasing wind speeds and was scarce on foggy days, presumably because terns rely in part on social facilitation to locate anchovy schools. The application of this intensive and non-invasive photo-sampling method revealed an important degree of foraging plasticity for this seabird within a context of locally reduced food availability, suggesting that, unlike species that specialise on a few high-quality prey, opportunistic seabirds may be better able to cope with reductions in the abundance of their preferred prey.

Group foraging in Socotra cormorants: A biologging approach to the study of a complex behavior.

Group foraging contradicts classic ecological theory because intraspecific competition normally increases with aggregation. Hence, there should be evolutionary benefits to group foraging. The study of group foraging in the field remains challenging however, because of the large number of individuals involved and the remoteness of the interactions to the observer. Biologging represents a cost-effective solution to these methodological issues. By deploying GPS and temperature-depth loggers on individuals over a period of several consecutive days, we investigated intraspecific foraging interactions in the Socotra cormorant Phalacrocorax nigrogularis, a threatened colonial seabird endemic to the Arabian Peninsula. In particular, we examined how closely birds from the same colony associated with each other spatially when they were at sea at the same time and the distance between foraging dives at different periods of the day. Results show that the position of different birds overlapped substantially, all birds targeting the same general foraging grounds throughout the day, likely following the same school of fish. There were as many as 44,500 birds within the foraging flock at sea at any time (50% of the colony), and flocking density was high, with distance between birds ranging from 8 to 1,380 m. Birds adopted a diving strategy maximizing time spent underwater relative to surface time, resulting in up to 72% of birds underwater in potential contact with prey at all times while foraging. Our data suggest that the benefits of group foraging outweigh the costs of intense aggregation in this seabird. Prey detection and information transmission are facilitated in large groups. Once discovered, shoaling prey are concentrated under the effect of the multitude. Fish school cohesiveness is then disorganized by continuous attacks of diving birds to facilitate prey capture. Decreasing population size could pose a risk to the persistence of threatened seabirds where group size is important for foraging success.

Defining ecologically relevant scales for spatial protection with long-term data on an endangered seabird and local prey availability.

Human activities are important drivers of marine ecosystem functioning. However, separating the synergistic effects of fishing and environmental variability on the prey base of nontarget predators is difficult, often because prey availability estimates on appropriate scales are lacking. Understanding how prey abundance at different spatial scales links to population change can help integrate the needs of nontarget predators into fisheries management by defining ecologically relevant areas for spatial protection. We investigated the local population response (number of breeders) of the Bank Cormorant (Phalacrocorax neglectus), a range-restricted endangered seabird, to the availability of its prey, the heavily fished west coast rock lobster (Jasus lalandii). Using Bayesian state-space modeled cormorant counts at 3 colonies, 22 years of fisheries-independent data on local lobster abundance, and generalized additive modeling, we determined the spatial scale pertinent to these relationships in areas with different lobster availability. Cormorant numbers responded positively to lobster availability in the regions with intermediate and high abundance but not where regime shifts and fishing pressure had depleted lobster stocks. The relationships were strongest when lobsters 20-30 km offshore of the colony were considered, a distance greater than the Bank Cormorant's foraging range when breeding, and may have been influenced by prey availability for nonbreeding birds, prey switching, or prey ecology. Our results highlight the importance of considering the scale of ecological relationships in marine spatial planning and suggest that designing spatial protection around focal species can benefit marine predators across their full life cycle. We propose the precautionary implementation of small-scale marine protected areas, followed by robust assessment and adaptive-management, to confirm population-level benefits for the cormorants, their prey, and the wider ecosystem, without negative impacts on local fisheries.

Can foraging ecology drive the evolution of body size in a diving endotherm?

Within a single animal species, different morphs can allow for differential exploitation of foraging niches between populations, while sexual size dimorphism can provide each sex with access to different resources. Despite being potentially important agents of evolution, resource polymorphisms, and the way they operate in wild populations, remain poorly understood. In this study, we examine how trophic factors can select for different body sizes between populations and sexes in a diving endotherm. Dive depth and duration are positively related to body size in diving birds and mammals, a relationship explained by a lower mass-specific metabolic rate and greater oxygen stores in larger individuals. Based on this allometry, we predict that selection for exploiting resources situated at different depths can drive the evolution of body size in species of diving endotherms at the population and sexual level. To test this prediction, we studied the foraging ecology of Blue-eyed Shags, a group of cormorants with male-biased sexual size dimorphism from across the Southern Ocean. We found that mean body mass and relative difference in body mass between sexes varied by up to 77% and 107% between neighbouring colonies, respectively. Birds from colonies with larger individuals dived deeper than birds from colonies with smaller individuals, when accounting for sex. In parallel, males dived further offshore and deeper than females and the sexual difference in dive depth reflected the level of sexual size dimorphism at each colony. We argue that body size in this group of birds is under intense selection for diving to depths of profitable benthic prey patches and that, locally, sexual niche divergence selection can exaggerate the sexual size dimorphism of Blue-eyed Shags initially set up by sexual selection. Our findings suggest that trophic resources can select for important geographic micro-variability in body size between populations and sexes.

Buoyancy under control: underwater locomotor performance in a deep diving seabird suggests respiratory strategies for reducing foraging effort.

BACKGROUND: Because they have air stored in many body compartments, diving seabirds are expected to exhibit efficient behavioural strategies for reducing costs related to buoyancy control. We study the underwater locomotor activity of a deep-diving species from the Cormorant family (Kerguelen shag) and report locomotor adjustments to the change of buoyancy with depth. METHODOLOGY/PRINCIPAL FINDINGS: Using accelerometers, we show that during both the descent and ascent phases of dives, shags modelled their acceleration and stroking activity on the natural variation of buoyancy with depth. For example, during the descent phase, birds increased swim speed with depth. But in parallel, and with a decay constant similar to the one in the equation explaining the decrease of buoyancy with depth, they decreased foot-stroke frequency exponentially, a behaviour that enables birds to reduce oxygen consumption. During ascent, birds also reduced locomotor cost by ascending passively. We considered the depth at which they started gliding as a proxy to their depth of neutral buoyancy. This depth increased with maximum dive depth. As an explanation for this, we propose that shags adjust their buoyancy to depth by varying the amount of respiratory air they dive with. CONCLUSIONS/SIGNIFICANCE: Calculations based on known values of stored body oxygen volumes and on deep-diving metabolic rates in avian divers suggest that the variations of volume of respiratory oxygen associated with a respiration mediated buoyancy control only influence aerobic dive duration moderately. Therefore, we propose that an advantage in cormorants--as in other families of diving seabirds--of respiratory air volume adjustment upon diving could be related less to increasing time of submergence, through an increased volume of body oxygen stores, than to reducing the locomotor costs of buoyancy control.