Adaptive strategies for post-renal handling of urine in birds

Birds are a diverse vertebrate class in terms of diet and habitat, but they share several common physiological features, including the use of uric acid as the major nitrogenous waste product and the lack of a urinary bladder. Instead, ureteral urine refluxes from the urodeum into the more proximal coprodeum and portions of the hindgut (colon or rectum and ceca). This presents a potential problem in that hyperosmotic ureteral urine in contact with the permeable epithelia of these tissues would counteract renal osmotic work. This review describes and provides examples of different strategies used by avian species to balance renal and post-renal changes in urine composition. The strategies described include: 1. a "reptilian" mode, with moderate renal concentrating ability, but high rates of post-renal salt and water resorption; 2. the "mammalian" strategy, in which the coprodeum effectively functions like a mammalian urinary bladder, preserving the osmotic concentrating work of the kidney; 3. an interaction strategy, in which post-renal transport processes are hormonally regulated in order to optimize renal function under varying conditions of salt or water stress; 4. the salt gland strategy seen in marine or estuarine birds with functional salt glands, in which post-renal transport mechanisms are used to conserve urinary water and to recycle excess NaCl to the nasal salt glands. Finally, we also describe some features of an as-yet unstudied group of birds, the birds of prey. At least some species in this group are relatively good renal concentrators, and would be predicted to have post-renal mechanisms to preserve this work. This new synthesis illustrates the marked diversity of adaptive mechanisms used by avian species to maintain osmotic homeostasis.     

Regulation of salt gland, gut and kidney interactions

Marine birds can drink seawater because their cephalic 'salt' glands secrete a sodium chloride (NaCl) solution more concentrated than seawater. Salt gland secretion generates osmotically free water that sustains their other physiological processes. Acclimation to saline induces interstitial water and Na move into cells. When the bird drinks seawater, Na enters the plasma from the gut and plasma osmolality (Osm(pl)) increases. This induces water to move out cells expanding the extracellular fluid volume (ECFV). Both increases in Osm(pl) and ECFV stimulate salt gland secretion. The augmented intracellular fluid content should allow more rapid expansion of ECFV in response to elevated Osm(pl) and facilitate activation of salt gland secretion. To fully utilize the potential of the salt glands, intestinally absorbed NaCl must be reabsorbed by the kidneys. Thus, Na uptake at gut and renal levels may constrain extrarenal NaCl secretion. High NaCl intake elevates plasma aldosterone concentration of Pekin ducks and aldosterone stimulates intestinal and renal water and sodium uptake. High NaCl intake induces lengthening of the small intestine of adult Mallards, especially males. High NaCl intake has little effect on glomerular filtration rate or tubular sodium Na uptake of birds with competent salt glands. Relative to body mass, kidney mass and glomerular filtration rate (GFR) are greater in birds with salt glands than in birds that do not have them. Birds with salt glands do not change GFR, when they drink saline. Thus, their renal filtrate contains excess Na that is, in some species, almost completely renally reabsorbed and excreted in a more concentrated salt gland secretion. Na reabsorption by kidneys of other species, like mallards is less complete and their salt glands make less concentrated secretion. Such species may reflux urine into the hindgut, where additional Na may also be reabsorbed for extrarenal secretion. During exposure to saline, marine birds maintain elevated aldosterone levels despite high Na intake. Marine birds are excellent examples of physiological plasticity.     

Osmoregulatory and metabolic costs of salt excretion in the Rufous-collared sparrow Zonotrichia capensis

Recent experiments on shorebirds have demonstrated that maintaining an active osmoregulatory machinery is energetically expensive. This may, in part, explain diet and habitat selection in birds with salt glands. However little is known about the osmoregulatory costs in birds lacking functional salt glands. In these birds, osmotic work is done almost exclusively by the kidneys. We investigated the osmoregulatory cost in a bird species lacking functional salt glands, the passerine Zonotrichia capensis. After 20 days of acclimation to fresh water (FW) and salt water (200 mM NaCl, SW), SW birds tended to be heavier than FW birds. However, this difference was not statistically significant. Total basal metabolic rate was higher in SW birds as compared with FW birds. Renal and heart masses were also higher in the SW group. We also found greater medullary development and an increase in urine osmolality in the SW group. In spite of Z. capensis' ability to tolerate a moderate salt load in the laboratory, we hypothesize that increased cost of maintenance produced by salt consumption may significantly affect energy budget, dietary, and habitat choices in the field.     

Excretory organ growth and implications for salt tolerance in hatchling American avocets Recurvirostra americana

The role of salt glands in avian osmoregulation has been widely studied. Acclimation to saline habitats in aquatic birds involves increases in the relative size and complexity of the salt glands, and it is generally agreed that salt gland size varies as a function of salt loading, and is broadly correlated with habitat salinity. We report here salt gland sizes in three age classes of American avocet Recurvirostra americana chicks. Mean relative (mg/g body mass) salt gland masses for newly hatched (<24 h old) avocet chicks collected at a wetland supplied with pumped fresh water was 0.48 mg salt gland/g body mass. This value is comparable to the low end of published values for some strictly marine birds and similar to values for adult American avocets collected at saline lakes. These results suggest that American avocets, which are frequently raised in saline environments, hatch with salt glands that are large enough to cope with the osmoregulatory demands of saline environments.     

Excretory organ growth and implications for salt tolerance in hatchling American avocets Recurvirostra americana

The role of salt glands in avian osmoregulation has been widely studied. Acclimation to saline habitats in aquatic birds involves increases in the relative size and complexity of the salt glands, and it is generally agreed that salt gland size varies as a function of salt loading, and is broadly correlated with habitat salinity. We report here salt gland sizes in three age classes of American avocet Recurvirostra americana chicks. Mean relative (mg/g body mass) salt gland masses for newly hatched (<24 h old) avocet chicks collected at a wetland supplied with pumped fresh water was 0.48 mg salt gland/g body mass. This value is comparable to the low end of published values for some strictly marine birds and similar to values for adult American avocets collected at saline lakes. These results suggest that American avocets, which are frequently raised in saline environments, hatch with salt glands that are large enough to cope with the osmoregulatory demands of saline environments.     

Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation

Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.     

Timing of fledging is influenced by glucocorticoid physiology in Laysan Albatross chicks

Fledging is a major life transition for birds, when juveniles move from the safety of a nest into an environment where they must find food and avoid predators. The timing of fledging within a season can have significant effects on future survival and breeding success. Proximate triggers of fledging are unknown: though wing development is likely a primary factor, other physiological changes, such as elevated plasma corticosterone (CORT), may affect fledging behavior. Laysan Albatross (Phoebastria immutabilis) chicks have an extended post−hatching period during which they reach 150% of adult mass. However, approaching fledging, chicks fast for days to weeks and lose mass while still putting energy into feather growth. We evaluated chick morphology and physiology to elucidate proximate triggers of fledging. As in some other species, CORT increased as chicks fasted and lost body mass. At the same time, corticosteroid binding globulin (CBG) declined, thus amplifying free CORT prior to fledging. Once chicks reached a morphological threshold, free CORT levels predicted how long they stayed at the colony: chicks with higher free CORT fledged sooner. To perturb the relationship between body condition, endocrine physiology, and fledging behavior, we supplementally fed chicks for the month before fledging. Fed birds had a slower decrease in body mass, slower decrease in CBG, slower increase in free CORT, and stayed at the colony longer after reaching a morphological threshold. Our study suggests that as chicks lose mass, free CORT acts as a signal of energetic or nutritional state to adjust the timing of fledging.     

Influence of proximity to a geographical range limit on the physiology of a tropical bird

1. Species' geographical ranges can be limited by a variety of biotic and abiotic factors. Physiological challenge in response to unsuitable environmental conditions can establish limits to geographical ranges. 2. We studied the physiology of Song Wrens (Cyphorhinus phaeocephalus) across their geographical range on the isthmus of Panama, an area characterized by a strong rainfall gradient. Wrens are common on the Caribbean slope of the isthmus where annual rainfall is greatest, but wren abundance declines towards the south as annual rainfall declines. Song Wrens are completely absent from the driest third of the isthmus. 3. We searched for the existence of a physiologically induced distribution limit by measuring body condition (an integrative measure of energy balance), hematocrit (% packed red blood cells in a given blood sample), and corticosterone levels (CORT, a steroid hormone that regulates the availability of energy and the endocrine stress response) in males and females. We caught birds by luring them into nets when they responded to playback of conspecific song. 4. Wrens living in drier habitat near the geographical range edge were significantly more likely to have abnormally low hematocrit scores. Baseline CORT levels were negatively associated with rainfall in one of our three best-fit path models, indicating potential energetic challenge in some individuals. Maximum CORT levels during a 60-min period of restraint correlated significantly only with sex, being higher in females. Birds with the poorest body condition lived at the dry end of the gradient. Birds on the wet end of the gradient responded fastest to conspecific song. 5. Environmental conditions vary across geographical ranges and may influence the physiological conditions of organisms, thereby enforcing limits to species' distributions. Highly specialized species, such as birds of the rain forest understory, may be especially susceptible to environmental variation associated with changing climatic conditions.     

Mediation of a corticosterone-induced reproductive conflict

Current research in birds suggests that a conflict should exist during reproduction for the role of the glucocorticoid corticosterone (CORT). While elevated levels have been correlated with the increased energetic demand of raising offspring, elevated CORT levels have traditionally been implicated in reproductive abandonment. We examined the relationship between CORT and nest desertion in breeding wild female European starlings (Sturnus vulgaris) incorporating analyses of both total circulating levels and 'free', unbound CORT through analysis of corticosteroid-binding globulin (CBG). Free baseline CORT levels of nest-abandoning birds were significantly higher than nonabandoning birds within each stage, with chick-rearing birds exhibiting the highest free baseline CORT levels, while concurrently remaining the most resistant stage to nest desertion. Elevated free baseline CORT levels in chick-rearing birds were not due to increased total CORT secretion, but rather to a decrease in CBG levels. Overall, our results suggest that CORT and CBG interact to play a role in mediating the increased energetic demand of offspring, while minimizing the chances of nest desertion, thereby alleviating any potential behavioral conflict for CORT during reproduction. Furthermore, these results demonstrate that the traditional view of the role of CORT during reproduction is much more complex than previously appreciated. Together with mounting evidence, we suggest that elevated corticosteroid levels are an inherent and necessary part of reproduction in nonmammalian tetrapods.     

Convergent evolution of sunbird pollination systems of Impatiens species in tropical Africa and hummingbird systems of the New World

The bird pollination systems of the New and Old Worlds evolved independently, and differ in many aspects. New World plants are often presented as those adapted to hovering birds while Old World plants to perching birds. Most Neotropical studies also demonstrate that in hummingbird species rich assemblages, only a small number of highly specialized birds exploits the most specialized plants with long corollas. Nevertheless, recent research on bird–plant pollination interactions suggest that sunbird pollination systems in the Old World have converged more with the highly specialized hummingbird pollination systems than previously thought. In this study we focus on the pollination systems of the bird pollination syndrome Impatiens species on Mt. Cameroon, West Africa. We show that despite the high diversity of sunbirds on Mt. Cameroon, only Cyanomitra oritis appear to be important pollinator of all Impatiens species. This asymmetry indicates the absence of pair wise co‐evolution and points to a diffuse co‐evolutionary process resulting in guilds of highly specialized plants and birds; a situation well known from hummingbirds and specialized plant communities of the New World. Additionally, the herbaceous habits of Impatiens species, the frequent adaptations to pollination by hovering birds, and the habitat preference for understory in tropical forests or epiphytic growth, resemble the highly specialized Neotropical plants. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 127–133.     

Immunolocalization of Na/K–ATPase and Na/K/2Cl cotransporter in the tubular epithelia of sea snake salt glands

The sublingual salt gland is the primary site of salt excretion in sea snakes; however, little is known about the mechanisms mediating ion excretion. Na⁺/K⁺–ATPase (NKA) and Na⁺/K⁺/2Cl⁻ cotransporter (NKCC) are two proteins known to regulate membrane potential and drive salt secretion in most vertebrate secretory cells. We hypothesized that NKA and NKCC would localize to the basolateral membranes of the principal cells comprising the tubular epithelia of sea snake salt glands. Although there is evidence of NKA activity in salt glands from several species of sea snake, the localization of NKA and NKCC and other potential ion transporters remains unstudied. Using histology and immunohistochemistry, we localized NKA and NKCC in salt glands from three species of laticaudine sea snake: Laticauda semifasciata, L. laticaudata, and L. colubrina. Antibody specificity was confirmed using Western blots. The compound tubular glands of all three species were found to be composed of serous secretory epithelia, and NKA and NKCC were abundant in the basolateral membranes. These results are consistent with the morphology of secretory epithelia found in the rectal salt glands of marine elasmobranchs, the nasal glands of marine birds and the gills of teleost fishes, suggesting a similar function in regulating ion secretion.     

Behavioural and physiological responses of birds to environmentally relevant concentrations of an antidepressant

Many wildlife species forage on sewage-contaminated food, for example, at wastewater treatment plants and on fields fertilized with sewage sludge. The resultant exposure to human pharmaceuticals remains poorly studied for terrestrial species. On the basis of predicted exposure levels in the wild, we administered the common antidepressant fluoxetine (FLUOX) or control treatment via prey to wild-caught starlings (Sturnus vulgaris) for 22 weeks over winter. To investigate responses to fluoxetine, birds were moved from their group aviaries into individual cages for 2 days. Boldness, exploration and activity levels showed no treatment effects but controls and FLUOX birds habituated differently to isolation in terms of the concentration of corticosterone (CORT) metabolites in faeces. The controls that excreted higher concentrations of CORT metabolites on day 1 lost more body mass by day 2 of isolation than those which excreted lower levels of CORT metabolites. CORT metabolites and mass loss were unrelated in FLUOX birds. When we investigated the movements of birds in their group aviaries, we found the controls made a higher frequency of visits to food trays than FLUOX birds around the important foraging periods of sunrise and sunset, as is optimal for wintering birds. Although individual variability makes interpreting the sub-lethal endpoints measured challenging, our data suggest that fluoxetine at environmentally relevant concentrations can significantly alter behaviour and physiology.     

The macroevolutionary relationship between diet and body mass across mammals

Body mass and diet are two fundamental ecological parameters that influence many other aspects of an animal's biology. Thus, the potential physiological and ecological processes linking size and diet have been the subject of extensive research, although the broad macroevolutionary relationship between the two traits remains largely unexplored phylogenetically. Using generalized Ornstein–Uhlenbeck models and data on over 1350 species of mammal, we reveal that evolutionary changes in body mass are consistently associated with dietary changes across mammals. Best‐fitting models find that herbivores are substantially heavier than other dietary groups and that omnivores are frequently intermediate in mass between herbivores and carnivores. Interestingly, although flying and swimming both place very different physical constraints on mass, bats still follow the general mammalian pattern but marine mammals do not. Such differences may be explained by reduced gravitational constraints on size in water along with ecological differences in food availability between aquatic and terrestrial realms, allowing marine carnivores to become the largest mammals on earth. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 173–184.     

Salt glands in a Tithonian metriorhynchid crocodyliform and their physiological significance

Our knowledge of Mesozoic tetrapods is based mainly on osteological evidence. The discussion of the evolution of any homeostatic system is highly speculative because direct non-osteological evidence is uncommon. Here we report an extraordinarily well-preserved cast of a pair of lobulated protuberances in the skull of the marine metriorhynchid crocodiliform Geosaurus from the Tithonian (Jurassic) of Patagonia (Argentina). These protuberances are interpreted as representing salt glands. Based on their topology, these glands are identified as the nasals. Optimization of this character on a phylogenetic tree permits us to infer the ancestral condition for archosaurs. The relationship between salt gland and diet is also analysed. The presence of hypertrophied salt glands in the skull of Geosaurus suggests that as early as 140 million years ago, some Mesozoic marine reptiles had evolved an extra-renal osmoregulatory system. This achievement was an important clue in the successful colonization of marine environments. Salt glands preclude the risk of lethal dehydration and allow marine reptiles to include an important amount of invertebrates in their diet.     

Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates

The femoral microanatomy of 155 species of extant amniotes (57 species of mammals, 15 species of turtles, 56 species of lepidosaurs, and 27 species of birds) of known lifestyle is studied to demonstrate a possible link between some basic parameters of bone structure and specific lifestyles, as well as phylogenetic relationships between taxa. Squared change parsimony with random taxon reshuffling and pairwise comparisons reveal that most compactness and size parameters exhibit both phylogenetic and ecological signals. A discriminant analysis produces several inference models, including a ternary model (aquatic, amphibious, terrestrial) that yield the correct lifestyle in 88% of the cases. These models are used to infer the lifestyle of three extinct Permian temnospondyls: Eryops megacephalus, Acheloma dunni, and Trimerorhachis insignis. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 644–655.     

Ancestry trumps experience: Transgenerational but not early life stress affects the adult physiological stress response

Exposure to stressors can affect an organism's physiology and behavior as well as that of its descendants (e.g. through maternal effects, epigenetics, and/or selection). We examined the relative influence of early life vs. transgenerational stress exposure on adult stress physiology in a species that has populations with and without ancestral exposure to an invasive predator. We raised offspring of eastern fence lizards (Sceloporus undulatus) from sites historically invaded (high stress) or uninvaded (low stress) by predatory fire ants (Solenopsis invicta) and determined how this different transgenerational exposure to stress interacted with the effects of early life stress exposure to influence the physiological stress response in adulthood. Offspring from these high- and low-stress populations were exposed weekly to either sub-lethal attack by fire ants (an ecologically relevant stressor), topical treatment with a physiologically-appropriate dose of the stress-relevant hormone, corticosterone (CORT), or a control treatment from 2 to 43 weeks of age. Several months after treatments ended, we quantified plasma CORT concentrations at baseline and following restraint, exposure to fire ants, and adrenocorticotropic hormone (ACTH) injection. Exposure to fire ants or CORT during early life did not affect lizard stress physiology in adulthood. However, offspring of lizards from populations that had experienced multiple generations of fire ant-invasion exhibited more robust adult CORT responses to restraint and ACTH-injection compared to offspring from uninvaded populations. Together, these results indicate that transgenerational stress history may be at least as important, if not more important, than early life stress in affecting adult physiological stress responses.     

Effects of population size and isolation on the genetic structure of the East African mountain white‐eye Zosterops poliogaster (Aves)

Habitat size, quality and isolation determine the genetic structure and diversity of populations and may influence their evolutionary potential and vulnerability to stochastic events. Small and isolated populations are subject to strong genetic drift and can lose much of their genetic diversity due to stochastic fixation and loss of alleles. The mountain white‐eye Zosterops poliogaster, a cloud forest bird species, is exclusively found in the high mountains of East Africa. We analysed 13 polymorphic microsatellites for 213 individuals of this species that were sampled at different points in time in three mountain massifs differing in habitat size, isolation and habitat degradation. We analysed the genetic differentiation among mountain populations and estimated the effective population sizes. Our results indicate three mountain‐specific genetic clusters. Time cohorts did not show genetic divergences, suggesting that populations are large enough to prevent strong drift effects. Effective population sizes were higher in larger and geographically interconnected habitat patches. Our findings underline the relevance of ecological barriers even for mobile species and show the importance of investigating different estimators of population size, including both approaches based on single and multiple time‐points of sampling, for the inference of the demographic status of a population. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 828–836.     

Does urbanization affect selective pressures and life‐history strategies in the common blackbird (Turdus merula L.)?

Urbanization, one of the most extreme land‐use alterations, is currently spreading, and the number of species confronting these changes is increasing. However, contradictory results of previous studies impede a clear interpretation of which selective pressure (nest predation or food limitation) is more important in urban habitats compared with natural situations, and whether birds can confront them by adjusting their life‐history strategies. We investigated life‐history syndromes of three common blackbird (Turdus merula) populations differing in their human influence (urban, rural, and woodland). We analysed daily nest predation and nestling starvation rates to assess the relative importance of these selection pressures in each habitat. Simultaneously, several life‐history traits were investigated to determine if T. merula seem adapted to their main source of selection. Food limitation was more important in the city, whereas nest predation was the most important selective force in the forest. The rural habitat was characterized by an intermediate influence of these two factors. Life‐history syndromes, as the covariation of a suite of traits, confirmed these results because T. merula seem well adapted to the main cause of selection in each habitat. Our results are consistent with urbanization imposing new challenges on birds, and that they adaptively respond to them. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 759–766.     

Epidermal glands in cordylid lizards,with special reference to generation glands

We investigated inter‐ and intraspecific variation in epidermal gland characteristics in cordylid lizards. Our particular interest was whether a causal relationship exists between the presence of generation glands and lifestyle, i.e. in rock‐dwelling or ground‐dwelling lizards. We established that both femoral and generation glands are always present in adult males, but that species can be divided into three categories on the basis of the presence of these glands in adult females: both femoral and generation glands absent; femoral glands present, but generation glands absent; and both femoral and generation glands present. The absence of epidermal glands in females appears to be the basal condition in the Cordylidae. All cordylid species are sexually dimorphic as far as generation gland number is concerned, with females having consistently less glands than males. Gland number in females is strongly affected by climate, being lower in cooler compared with warmer environments. In males, there is no clear geographical pattern, although in some clades males of high‐altitude species have more generation glands than males of species occurring at lower altitudes. At least four of the five ground‐dwelling species in the family display unique generation gland characteristics, compared with rock‐dwelling species, reflecting the continued importance of generation glands in terrestrial environments. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 312–324.     

Variation in adrenocortical stress physiology and condition metrics within a heterogeneous urban environment in the song sparrow Melospiza melodia

In urban habitats, organisms face unique fitness challenges including disturbance from human activity and noise. One physiological mechanism that may be plastically or evolutionarily modified to ameliorate deleterious effects of anthropogenic disturbance is the adrenocortical stress response. Individuals in urban environments may display smaller stress responses, which may prevent pathologies associated with consistent elevation of stress hormones, and may also show differences in baseline corticosterone (CORT, the primary avian stress hormone), due to altered energetic demands or chronic stress. We examined whether stress physiology and condition metrics in male song sparrows Melospiza melodia vary as a function of discrete differences in anthropogenic disturbance level (activity centers and refuges) or with continuous variation in an urbanization score and noise environment. Males breeding in activity centers displayed lower maximal (acute) CORT levels than activity refuge males, and acute CORT also tended to negatively correlate with urbanization score. Baseline CORT did not differ between habitat types, and activity center males also showed no evidence of changes in body mass, hematocrit, or antioxidant capacity. Further, activity center males had higher quality feathers (indicative of higher condition at molt) than activity refuge males. We found no indication that the noise environment altered stress physiology or condition in song sparrows. Overall, results suggest that song sparrows are an urban adapter species, which are not detrimentally affected by unique selective pressures encountered in the urban environment.