Juan M. Sánchez-Guzmán

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.

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.

Assessing the role of multiple environmental factors on Eurasian Spoonbill departure decisions from stopover sites

Understanding the factors driving departure decisions from stopover sites is critical when predicting the dynamics of bird migration. We Investigated the Interactive effects of wind, tidal characteristics, and precipitation on the departure decisions of the Eurasian Spoonbill Platalea l. leucorodia from a major coastal stopover locality in northern Iberia. Most departing Spoonbills (>80%) crossed an adjacent mountain range to follow a direct route over Inland Iberia, while the remainder made a detour following an Indirect coastal route along the coast of the Iberian Peninsula. During four consecutive autumns, we daily monitored departing Spoonbills leaving along these two routes. The birds taking the Inland route, crossing unsuitable habitats and needing therefore higher fuel-loads, departed preferentially under favourable tailwind conditions (TWC). This represented a significant increase in distance covered and/or a decrease in energy spent per unit time. Moreover, Spoonbills taking the inland route often departed during spring tides. For the indirect coastal route, TWC did not affect the onset of migration but bird departures increased with neap tides. Precipitation and date were negatively correlated with departures towards both routes, whereas Spoonbill density at the stopover had a positive effect. Our findings provide empirical support for the role that wind assistance may play for Spoonbills to resume migration.

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.

Effects of Diet on Growth-Related Patterns of Energy and Macronutrient Assimilation Efficiency in a Semi-Precocial Bird, the Gull-Billed Tern Gelochelidon nilotica

Albano N., Masero J.A., Sánchez-Guzmán J.M., Villegas A. & Santiago-Quesada F. 2011. Effects of diet on growth-related patterns of energy and macronutrient assimilation efficiency in a semi-precocial bird, the Gull-billed Tern Gelochelidon nilotica. Ardea 99: 93–101. Despite the extensive literature on energy assimilation efficiency in birds, only a few studies have dealt specifically with offspring, and to our knowledge there is no information on macronutrient assimilation efficiencies during the growth period of chicks. We studied growth-related energy and macronutrient assimilation efficiencies of semi-precocial chicks of Gull-billed Terns Gelochelidon nilotica as a function of their diet. We experimentally evaluated several digestive parameters in chicks fed different diets — fish vs. insects — when 10, 15 and 22 days old. Gross daily energy intake was similar in the two groups throughout the growth period, but fish-fed chicks showed consistently higher energy and macronutrient assimilation efficiencies than chicks fed insects. Energy and macronutrient assimilation efficiencies varied with age, peaking at 15 days old. The only digestive parameter that did not decrease during the last phase of growth was the lipid assimilation efficiency. Fish-fed chicks grew significantly faster than those fed on insects, which showed delayed growth. We suggest that semi-precocial chicks could modulate energy and macronutrient assimilation efficiency according to their growth requirements and that such digestive parameters can help us to understand differences in chick growth rates and breeding success in a natural environment.

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.

Sex-specific vulnerability to breeding conditions in chicks of the sexually monomorphic Gull-billed Tern

AbstractEnvironmental conditions during early development may differentially affect male and female offspring, and the effects of this sex–environment interaction in chick performance may be exaggerated under harsh conditions. In birds, most of the currently available evidence on sex-biased environmental sensitivity in nestlings is derived from species that display sexual size dimorphism, while studies on monomorphic or slightly dimorphic species are less abundant and have produced inconsistent results. We have evaluated sex-specific vulnerability to breeding conditions in chicks of the Gull-billed Tern (Gelochelidon nilotica), a semiprecocial species with only low sexual size dimorphism. We compared male and female mass growth and fledgling physiological condition (measured through plasma metabolite levels) in several colonies that differed in reproductive parameters. Chicks of both sexes grew more slowly and fledged with lower mass and poorer nutritional state in the colony with the worst breeding conditions, i.e., with later phenology and lower clutch size and reproductive success. Contrary to our expectations, chick vulnerability to rearing conditions was more pronounced for female than male fledglings. While males grew faster than females during the middle phase of growth regardless of colony, this difference disappeared later in the fledging period in all but the worst colony, where females maintained a lower mass and worse nutritional condition than males. These results add to the evidence that, even in monomorphic species, the environmental sensitivity of nestlings during development may vary in a sex-specific way that may select for sex-biased allocation of parental resources and sex ratio adjustments under specific breeding conditions.ZusammenfassungGeschlechtsspezifische Anfälligkeit gegen Aufzuchtsbedingungen bei Küken eines sexuell monomorphen Vogels, der Lachseeschwalbe Die Umweltbedingungen während der frühen Entwicklung können männliche und weibliche Nachkommen unterschiedlich beeinflussen, und diese Geschlechts-Umwelt-Interaktion in der Kükenperformanz kann unter harschen Bedingungen verstärkt sein. Bei Vögeln stammen die meisten Belege für geschlechtsspezifische Umweltempfindlichkeit aus Arten mit sexuellem Größendimorphismus, während Untersuchungen an monomorphen oder nur leicht dimorphen Arten seltener sind und widersprüchliche Ergebnisse erbracht haben. Hier schätzen wir die geschlechtsspezifische Anfälligkeit gegen die Aufzuchtsbedingungen bei Küken der Lachseeschwalbe (Gelochelidon nilotica) ab, einer halb-nestflüchtenden Art mit nur geringem sexuellen Größendimorphismus. Wir haben den Körpermassezuwachs von Männchen und Weibchen und ihre physiologische Kondition als Flügglinge (gemessen über den Plasmametabolitspiegel) in mehreren Kolonien, die sich in Fortpflanzungsparametern unterschieden, verglichen. Küken beiden Geschlechts wuchsen langsamer und wiesen beim Ausfliegen eine geringere Körpermasse und einen schlechteren Ernährungszustand auf in der Kolonie mit den schlechtesten Brutbedingungen, d.h. mit späterer Phänologie, kleinerer Gelegegröße und niedrigerem Fortpflanzungserfolg. Entgegen unserer Erwartungen waren weibliche Küken empfindlicher gegen die Aufzuchtsbedingungen als männliche. Während Männchen in der mittleren Wachstumsphase schneller wuchsen als Weibchen, unabhängig von der Kolonie, verschwand dieser Unterschied später in der Ausflugsperiode in allen Kolonien außer der schlechtesten, wo Weibchen weiterhin eine geringere Körpermasse und einen schlechteren Ernährungszustand als Männchen aufwiesen. Diese Ergebnisse liefern weitere Belege, dass selbst bei monomorphen Arten die Umweltempfindlichkeit der Nestlinge während der Entwicklung geschlechtsspezifisch variieren kann, was unter bestimmten Brutbedingungen eine verstärkte Zuteilung elterlicher Ressourcen zu einem Geschlecht sowie eine Anpassung des Geschlechterverhältnisses der Nachkommen begünstigen kann.

Persistent bimodal activity patterns in wild and captive black-tailed godwit Limosa limosa under different environmental conditions

There is a large literature dealing with daily foraging routines of wild birds during the non-breeding season. While different laboratory studies have showed that some bird activity patterns are a persistent property of the circadian system, most of field studies preclude the potential role of an endogenous circadian rhythm in controlling bird’s foraging routines. In this study we compared the patterns of diurnal foraging activity and intake rates of migrating black-tailed godwits, Limosa limosa (radio-tagged and non-tagged individuals) at two stopover sites (habitats) with different environmental characteristics, aiming at identifying proximate factors of bird activity routines. To gain insights into the role of food availability in control of such foraging routines, we also estimated foraging activity patterns in captive godwits subjected to constant food availability. Captive and wild black-tailed godwits showed a persistent bimodal activity pattern through daylight period. Food availability had a significant effect on the intake rates, but had a subtler effect on foraging and intake rate rhythms. Temperature and wind speed (combined in a weather index) showed non-significant effects on both rhythms. Although we could not discard a role for natural diurnal changes in light intensity, an important timing cue, our findings support the idea that an endogenous circadian rhythm could be an important proximate factor regulating foraging activity and food items taken per unit time of wild black-tailed godwits during migration.

Behavioural Plasticity in Foraging Mode of Typical Plovers

The foraging behaviour of typical plovers is highly stereotyped, and short-billed plovers all forage visually in a run—stop—search manner. To date, the use of a sandpiper-like foraging method by typical plovers is considered anecdotal in non-breeding plovers, since only one study has described Grey Plovers Pluvialis squatarola foraging as sandpipers do, striding slowly and pecking at the water surface during short periods. We studied the behaviour and intake rate of Grey and Ringed Plovers Charadrius hiaticula foraging like sandpipers on suspended prey items in the water column of hypersaline pans, and investigated factors that may influence their occurrence. The feeding rate was 48.9 ± 18.0 (SD) and 19.1 ± 6.3 prey min-1 for Ringed and Grey Plover, respectively. For Ringed Plovers, the net intake rate was 0.23 ±0.05 kJ min-1, and for Grey Plovers 0.09 ± 0.01 kJ min-1. The sandpiper-like foraging method was particularly important for Ringed Plovers, since up to 24% of the population foraged in this way at high tide. We found that the sandpiper-like foraging method is a common foraging method in Ringed Plover feeding in prey-abundant pans and is occasionally used by Grey Plovers as well. We showed that behavioural plasticity in foraging methods of typical plovers may be greater than has been assumed previously. These results suggest that typical plovers can successfully locate and capture small prey items while walking continuously and without the need to stop to improve visual acuity.