17 Oct 2012
Physiological adjustments of migratory shorebirds to osmotic and immune challenges

BRANTA — Jorge S. Gutiérrez

Physiological adjustments of migratory shorebirds to osmotic and immune challenges

Institution: Conservation Biology Research Group, University of Extremadura, Spain
Supervisors: José A. Masero & Juan M. S├ínchez-Guzm├ín
Details: PhD 2012 (Completed)

Address: Conservation Biology Research Group, Department of Anatomy, Cell Biology and Zoology, Faculty of Sciences, University of Extremadura, Avenida de Elvas, 06006 Badajoz, Spain (Oct 2012) Email

Subject Keywords: energetics, habitat selection, immune response, life history trade-offs, metabolic rates, migration, osmotic balance, phenotypic flexibility, salinity, shorebirds
Species Keywords: Dunlin, Calidris alpina, Red knot, Calidris canutus, Bar-tailed godwit, Limosa lapponica, Little ringed plover Charadrius dubius



The main aim of this thesis is to provide insight into how migratory shorebirds (suborder Charadrii) cope with osmotic and immune challenges from an ecophysiological perspective. To do so, changes in a range of physiological traits including basal metabolic rate (BMR), energy consumption, body mass, fat stores, immune responses, concentration of ions in plasma, and the mass of specific organs were studied under different environmental conditions (Chapter 1).

Most migratory shorebirds spend a great deal of their time in coastal saline habitats where they must deal with high physiological salt loads. To cope with salt stress, they have a powerful 'osmoregulatory machinery', which is thought to be expensive to use and maintain. The energetic costs of living in saline environments were assessed in dunlins Calidris alpina acclimated to different salinities (Chapter 2). As expected, dunlins increased their BMR and daily energy consumption with salinity, reflecting significant osmoregulatory costs. Also, the relatively low body mass of dunlins coping with osmotically challenging environments suggests that this might be part of an adaptative response to maximize energy savings. Accordingly, it was emphasized that osmoregulatory costs should be integrated more fully into future foraging and energetics studies of shorebirds in marine, coastal, and estuarine systems.

The supraorbital (nasal) saltglands are the principal excretory route for excess salt in shorebirds. These glands extract salt ions from the bloodstream and produce a concentrated salt solution that is discarded through the nostrils. Previous studies have shown that both the size and excretory capacity of these organs vary as a function of habitat salinity and dietary salt. However, saltgland size is not always correlated with these factors, and often shows marked seasonal variation. Here, it was examined how climate conditions, prey type, and energy requirements affected the saltgland mass of shorebirds by making comparisons across and within 29 species of shorebirds that differ in habitat, diet and ambient temperatures (Chapter 3). For a more detailed picture of the importance of energy requirements and ambient temperature in saltgland mass, comparisons were focused on two long-distance migrants with a world-wide distribution (red knot Calidris canutus and bar-tailed godwit Limosa lapponica). The results supported the notion that habitat salinity and dietary salt content to a large extent explain variation in saltgland size. When considering marine species only, mollusc-eaters had larger saltglands than those eating non-shelled prey, indicating that seawater contained within the shells added to the salt load. In both bar-tailed godwits and red knots, saltgland mass was positively correlated with intestine mass, an indicator of relative food intake rates (salt loads). Additionally, red knots showed an increase in saltgland mass at both low and high temperatures, which probably reflects increased energy demand for thermoregulation at low temperatures and elevated respiratory water loss at high temperatures. Therefore, it can be concluded that shorebirds adjust the mass of this small but essential piece of metabolic machinery to successfully overcome the osmoregulatory challenges faced in the course of their annual cycles.

Despite growing evidence that mounting immune responses is an energetically costly activity in birds, such costs are virtually unknown in migratory birds. In this context, it was investigated whether little ringed plovers Charadrius dubius immuno-challenged with phytohaemagglutinin (PHA) would display different metabolic adjustments as a function of food availability (Chapter 4). It was found that plovers eating at will increased their BMR and inflammatory response when injected with PHA, whereas plovers coping with a food-restriction-immune-response overlap experienced a BMR downregulation and mounted a weaker inflammatory response. Both responses might be considered energy-saving mechanisms to maintain the body mass above a critical level and maximize fitness. Knowing this, and that salinity conditions change the immune function in many aquatic animals, it was hypothesized that salinity could also have an effect on the strength and cost of mounting an immune response in shorebirds (Chapter 5). This question was investigated by measuring the PHA-induced skin swelling, BMR, body mass, fat stores, and plasma ions of dunlins acclimated to either freshwater or seawater. Seawater-acclimated dunlins mounted a PHA-induced swelling response much weaker than those held under freshwater conditions. Freshwater-acclimated dunlins injected with PHA increased their relative BMR, whereas seawater-acclimated dunlins did not. However, this differential immune and metabolic response between freshwater- and seawater-acclimated dunlins was not associated with significant changes in body mass, fat stores or plasma ions. These results indicate that the strength of the immune response of this small-sized migratory shorebird was negatively influenced by the salinity of marine habitats and that the trade-off between osmoregulation and immune responsiveness might not be based on energy or nutrient limitation.

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 offer a particularly interesting opportunity for testing this difference, as they are typically divided into two broad categories in terms of their non-breeding habitat occupancy: 'coastal' and 'inland' shorebirds. BMRs for 12 species of migratory shorebirds wintering in temperate inland habitats were measured and additional BMR values for coastal and inland shorebirds were collected from the literature to make interspecific comparisons (Chapter 6). This study provided empirical evidence supporting the notion that inland species have lower BMRs than coastal species. The interspecific analyses showed that BMR is lower in inland shorebirds after the effects of climatic and organismal factors were accounted for. It was proposed that physical and biotic characteristics (absence of tidally-induce food restrictions, low salinity of prey and drinking water, less windy microclimates, and lower productivity) associated with inland freshwater habitats may reduce the levels of energy expenditure, and hence BMR.

When all the physiological adjustments presented in this thesis are jointly considered, it follows that shorebirds adopt diverse physiological strategies to deal with osmotic and immune challenges (Chapter 7).


Published papers

Jorge S. Gutiérrez, José A. Masero, José M. Abad-Gómez, Auxiliadora Villegas & Juan M. S├ínchez-Guzm├ín. 2011. 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. Journal of Experimental Biology 214: 829-835. View paper
Jorge S. Gutiérrez, José A. Masero, José M. Abad-Gómez, Auxiliadora Villegas & Juan M. S├ínchez-Guzm├ín. 2011, Metabolic consequences of overlapping food restriction and cell-mediated immune response in a long-distance migratory shorebird, the little ringed plover Charadrius dubius. Journal of Avian Biology 42: 259-265. View abstract
Jorge S. Gutiérrez, Maurine W. Dietz, José A. Masero, Robert E. Gill, Jr, Anne Dekinga, Phil F. Battley, Juan M. S├ínchez-Guzm├ín & Theunis Piersma. 2012. Functional ecology of saltglands in shorebirds: flexible responses to variable environmental conditions. Functional Ecology 26: 236-244. View abstract
Jorge S. Gutiérrez, José M. Abad-Gómez, Auxiliadora Villegas, Juan M. S├ínchez-Guzm├ín & José A. Masero. 2012. Effects of salinity on the immune response of an 'osmotic generalist' bird. Oecologia. View abstract
Jorge S. Gutiérrez, José M. Abad-Gómez, Juan M. S├ínchez-Guzm├ín, Juan G. Navedo & José A. Masero. 2012. Avian BMR in marine and non-marine habitats: a test using shorebirds. PLoS ONE 7: e42206. View abstract

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