José M. Abad-Gómez

Understanding the energetic costs of living in saline environments: effects of salinity on basal metabolic rate, body mass and daily energy consumption of a long-distance migratory shorebird

SUMMARY Many migratory vertebrates typically move between habitats with varying salinities during the annual cycle. These organisms clearly exhibit a remarkable phenotypic flexibility in their ‘osmoregulatory machinery’, but the metabolic consequences of salinity acclimatization are still not well understood. We investigated the effects of salinity on basal metabolic rate (BMR), body mass and daily energy consumption of a long-distance migratory shorebird, the dunlin (Calidris alpina), outside the breeding season. Mass-corrected BMR and daily energy consumption increased significantly by 17 and 20% between freshwater (0.3‰ NaCl) and saltwater (33.0–35.0‰ NaCl), respectively. Body mass in both captive and wild dunlins was lower (9–16%) in saline than in freshwater environments. These changes on BMR and body mass were quickly reversed by returning the birds to freshwater, suggesting that metabolic adjustment to saltwater and metabolic readjustment to freshwater are both processes that occur in a few days. Our findings support empirically that the processes of developing and maintaining an active osmoregulatory machinery are energetically expensive, and they could help to explain diet and/or habitat selection patterns along the flyway. Finally, we discuss whether body mass loss in saltwater may be a strategy to reduce maintenance cost in osmotically stressful conditions such as overwintering in marine habitats, and raise some methodological implications for studies of BMR-related outcomes using captive birds captured in saline environments.

When Siberia came to the Netherlands : The response of continental black-tailed godwits to a rare spring weather event

1. Extreme weather events have the potential to alter both short- and long-term population dynamics as well as community- and ecosystem-level function. Such events are rare and stochastic, making it difficult to fully document how organisms respond to them and predict the repercussions of similar events in the future. 2. To improve our understanding of the mechanisms by which short-term events can incur long-term consequences, we documented the behavioural responses and fitness consequences for a long-distance migratory bird, the continental black-tailed godwit Limosa limosa limosa, resulting from a spring snowstorm and three-week period of record low temperatures. 3. The event caused measurable responses at three spatial scales - continental, regional and local - including migratory delays (+19 days), reverse migrations (>90 km), elevated metabolic costs (+8·8% maintenance metabolic rate) and increased foraging rates (+37%). 4. There were few long-term fitness consequences, however, and subsequent breeding seasons instead witnessed high levels of reproductive success and little evidence of carry-over effects. 5. This suggests that populations with continued access to food, behavioural flexibility and time to dissipate the costs of the event can likely withstand the consequences of an extreme weather event. For populations constrained in one of these respects, though, extreme events may entail extreme ecological consequences.

Long lengths of stay, large numbers, and trends of the Black-tailed Godwit Limosa limosa in rice fields during spring migration

Rice fields provide functional wetlands for declining shorebirds and other waterbirds around the world, but fundamental aspects of their stopover ecology in rice fields remain unknown. We estimated the length of stay of Black-tailed Godwits Limosa limosa migrating through rice fields, and showed the international importance of Extremadura’s rice fields (south-west Spain) for this Near Threatened shorebird species. Overall, large numbers of Black-tailed Godwits en route to their breeding grounds had long lengths of stay in the rice fields (34.7 ± 1.7, 14.4 ± 2.0 and 8.3 ± 1.2 days in godwits radio-tagged in late January, early February, and late February, respectively). The long lengths of stay of godwits in rice fields, together with some aspects of their feeding ecology, suggest that rice fields are suitable staging habitats, and therefore they could play an important role as buffer habitats against the loss or degradation of natural wetlands. Extremadura’s rice fields supported at least 14% of the declining Western European population of Black-tailed Godwit, and its increasing number in south-west Spain probably reflects a population shift towards the northern part of the winter range. We strongly suggest the inclusion of Extremadura’s rice fields as a Special Protection Area for birds under the European Union Directive on the conservation of wild birds.

Avian BMR in marine and non-marine habitats: a test using shorebirds.

Basal metabolic rate (BMR) is closely linked to different habitats and way of life. In birds, some studies have noted that BMR is higher in marine species compared to those inhabiting terrestrial habitats. However, the extent of such metabolic dichotomy and its underlying mechanisms are largely unknown. Migratory shorebirds (Charadriiformes) offer a particularly interesting opportunity for testing this marine–non-marine difference as they are typically divided into two broad categories in terms of their habitat occupancy outside the breeding season: ‘coastal’ and ‘inland’ shorebirds. Here, we measured BMR for 12 species of migratory shorebirds wintering in temperate inland habitats and collected additional BMR values from the literature for coastal and inland shorebirds along their migratory route to make inter- and intraspecific comparisons. We also measured the BMR of inland and coastal dunlins Calidris alpina wintering at a similar latitude to facilitate a more direct intraspecific comparison. Our interspecific analyses showed that BMR was significantly lower in inland shorebirds than in coastal shorebirds after the effects of potentially confounding climatic (latitude, temperature, solar radiation, wind conditions) and organismal (body mass, migratory status, phylogeny) factors were accounted for. This indicates that part of the variation in basal metabolism might be attributed to genotypic divergence. Intraspecific comparisons showed that the mass-specific BMR of dunlins wintering in inland freshwater habitats was 15% lower than in coastal saline habitats, suggesting that phenotypic plasticity also plays an important role in generating these metabolic differences. We propose that the absence of tidally-induced food restrictions, low salinity, and less windy microclimates associated with inland freshwater habitats may reduce the levels of energy expenditure, and hence BMR. Further research including common-garden experiments that eliminate phenotypic plasticity as a source of phenotypic variation is needed to determine to what extent these general patterns are attributable to genotypic adaptation.

International importance of Extremadura, Spain, for overwintering migratory dabbling ducks: a role for reservoirs.

Many migratory waterbird populations are in decline and loss of natural wetlands is one of the main causes.However, some speciesmay respondpositively to artificial wetland recreation. In Extremadura (south-west Europe), several large reservoirs were created for irrigation since the 1960s and some comparatively small reservoirs were built from the late 1990s onwards close to rice fields. Here we analyse the abundance of wintering dabbling ducks (Anas spp.) in Extremadura before (1991–1994) and after (2007–2010) the creation of these new reservoirs in order to address the current importance of the area for this guild within the East Atlantic Flyway (EAF). A mean of 25,277 dabbling ducks wintered in the study area during 1991–1994, increasing to 46,163 individuals during 2007–2010. After controlling for environmental variables, Northern Pintail Anas acuta, Common Teal A. crecca and Northern Shoveler A. clypeata experienced significant increases in the area between both periods, and only Eurasian Wigeon A. penelope suffered a significant decrease. Mallard A. platyrhynchos and Gadwall A. strepera populations did not show any significant trend. The large older reservoirs experienced overall population decreases between the two periods, with four new reservoirs holding more than 35,000 wintering dabbling ducks. Our results reflect an overall improvement in habitat conditions, driven by the creation of reservoirs near to rice fields that could have resulted in a partial redistribution of wintering dabbling ducks in the EAF. The area emerges as one of the most important wintering sites for dabbling ducks in southern Europe, regularly exceeding two of the Ramsar Convention criteria for the conservation of several populations. The protection of these new reservoirs by legal mechanisms would guarantee the existence of a large functional wetland area, which could also mitigate the loss of natural wetlands for populations using the EAF.

Time Course and Metabolic Costs of a Humoral Immune Response in the Little Ringed Plover Charadrius dubius

Despite host defense against parasites and pathogens being considered a costly life-history trait, relatively few studies have assessed the energetic cost of immune responsiveness. Knowledge of such energetic costs may help to understand the mechanisms by which trade-offs with other demanding activities occur. The time course and associated metabolic costs of mounting a primary and secondary humoral immune response was examined in little ringed plovers Charadrius dubius challenged with sheep red blood cells. As was expected, the injection with this antigen increased the production of specific antibodies significantly, with peaks 6 d postinjection in both primary and secondary responses. At the peak of secondary antibody response, the antibody production was 29% higher than that observed during the primary response, but the difference was nonsignificant. Mounting the primary response did not significantly increase the resting metabolic rate (RMR) of birds, whereas the secondary response did by 21%, suggesting that the latter was more costly in terms of RMR. In spite of the fact that the primary response did not involve an increase in RMR, birds significantly decreased their body mass. This could imply an internal energy reallocation strategy to cope with the induced immune challenge. Last, we found that RMR and antibody production peaks were not coupled, which could help to conciliate the variable results of previous studies. Collectively, the results of this study support the hypothesis that humoral immunity, especially the secondary response, entails energetic costs that may trade-off with other physiological activities.

Wetland salinity induces sex-dependent carry-over effects on the individual performance of a long-distance migrant

Salinization is having a major impact on wetlands and its biota worldwide. Specifically, many migratory animals that rely on wetlands are increasingly exposed to elevated salinity on their nonbreeding grounds. Experimental evidence suggests that physiological challenges associated with increasing salinity may disrupt self-maintenance processes in these species. Nonetheless, the potential role of salinity as a driver of ecological carry-over effects remains unstudied. Here, we investigated the extent to which the use of saline wetlands during winter – inferred from feather stable isotope values – induces residual effects that carry over and influence physiological traits relevant to fitness in black-tailed godwits Limosa limosa limosa on their northward migration. Overwintering males and females were segregated by wetland salinity in West Africa, with females mostly occupying freshwater wetlands. The use of these wetlands along a gradient of salinities was associated with differences in immune responsiveness to phytohaemagglutinin and sized-corrected body mass in godwits staging in southern Europe during northward migration – 3,000 km from the nonbreeding grounds – but in males only. These findings provide a window onto the processes by which wetland salinity can induce carry-over effects and can help predict how migratory species should respond to future climate-induced increases in salinity.