Resumen de Ajustes fisiológicos en aves limícolas migratorias ante retos osmóticos e inmunológicos
An organism¿s ability to adjust its physiological traits to changes in environmental conditions is central for its ecological success. Due to their highly migratory nature and diverse ecological characteristics, shorebirds (also known as waders; Charadriiformes) are a robust model system with which to explore the complex interactions between organism and environment. The main aim of this thesis is to provide insight into how migratory shorebirds cope with osmotic and immune challenges within the framework of energetics. To do so, we look at changes in a range of physiological traits including basal metabolic rate (BMR), daily energy consumption, body mass, fat stores, immune responses, concentrations of ions in plasma, and the mass of specific organs (the saltglands) (Chapter 1).
Most migratory shorebirds spend a great deal of their time in coastal habitats, where they feed on marine invertebrates, and subsequently 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. We investigated the energetic costs of living in saline environments for dunlins Calidris alpina acclimated to different salinities (Chapter 2). As expected, dunlins increased their mass-specific BMR and daily energy consumption with salinity, reflecting significant osmoregulatory costs. Also, the relatively low body mass of both captive and wild dunlins coping with osmotically challenging environments suggests that this trait might be part of an adaptative response to maximize energy saving. We emphasize that osmoregulatory costs should be integrated more fully into future foraging and energetics studies of shorebirds ¿and other waterbirds¿ in marine, coastal, and estuarine systems.
Located on the skull between eyes, 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. Excreted salt may be visible as `water¿ drips off the tip of the beak. Previous studies have shown that both the size and excretory capacity of these organs vary as a function of habitat salinity and dietary salt; that is, saltglands are larger and more efficient in species and individuals that have higher salt loads. However, saltgland size is not always correlated with these factors, and often shows marked seasonal variation. Here, we went one step further and examined how climatic conditions, prey type, and energy requirements affected the saltgland mass of shorebirds (Chapter 3). We made comparisons across and within 29 species of shorebirds that differ in habitat, diet and ambient temperatures. For a more detailed picture of the importance of energy requirements and ambient temperature in saltgland mass, we focused on two long-distance migrants with a world-wide distribution (red knot Calidris canutus and bar-tailed godwit Limosa lapponica). Our results supported the notion that habitat salinity and dietary salt content to a large extent explains 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. We can conclude 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, often generating physiological trade-offs with other energy-demanding processes, such costs are virtually unknown in migratory birds. In this context, we investigated whether little ringed plovers Charadrius dubius challenged with phytohaemagglutinin (PHA) displayed different metabolic adjustments as a function of food availability (Chapter 4). We found that plovers eating without food restriction 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 the BMR downregulation and the reduced inflammatory response observed in birds facing such an overlap could be energy-saving mechanisms to maintain the body mass above a critical level and maximize fitness. These results further confirm the notion that when traits are affected by two or more ecological variables simultaneously, these may generate opposite responses compared to when they act separately.
Knowing that salinity conditions change the immune function in many aquatic animals, we hypothesized that salinity could also have an effect on the strength and cost of mounting an immune response in dunlins (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 that was 17% weaker than those held under freshwater conditions, despite ad libitum access to food. 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. Further, we suggest that the trade-off between salinity and immunocompetence might not only be based on energy or nutrient limitation, but also on a variety of mechanisms including modulation of the immune system by osmoregulatory hormones.
In birds, some studies have noted that BMR is higher in marine species compared to those inhabiting terrestrial habitats and vice versa. 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. 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 interspecific comparisons (Chapter 6). We present some 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 (latitude, temperature, solar radiation, and wind conditions) and organismal (body mass, migratory status, and phylogeny) factors were accounted for. We propose that physical and biotic characteristics 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 different physiological strategies to deal with osmotic and immune challenges (Chapter 7). This fact illustrates the complex interplay between ecological factors and physiological flexibility, which ultimately determine an organism¿s fitness. We conclude that the pronounced phenotypic flexibility in BMR and other physiological traits enables shorebirds to survive in their highly variable environments.
