Light at night reduces digestive efficiency of developing birds: an experiment with king quail.

Artificial light at night (ALAN) exposes animals to a novel environmental stimulus, one that is generally thought to be maladaptive. ALAN-related health problems have received little attention in non-model species, and we generally know little about the nutritional-physiological impacts of ALAN, especially in young animals. Here, we use a novel application of the acid steatocrit method to experimentally assess changes in digestive efficiency of growing king quail (Excalfactoria chinensis) in response to ALAN. Two weeks after hatching, quail were split into two groups (n = 20-21 per group): overnight-light-treated vs. overnight-dark-treated. When the chicks were 3 weeks old, the experimental group was exposed to weak blue light (ca. 0.3 lux) throughout the entire night for 6 consecutive weeks, until all the chicks had achieved sexual maturation. Fecal samples for assessing digestive efficiency were collected every week. We found that digestive efficiency of quail was reduced by ALAN at two time points from weeks 4 to 9 after hatching (quail reach adulthood by week 9). The negative effect of ALAN on digestion coincided with the period of fastest skeletal growth, which suggests that ALAN may reduce digestive efficiency when energetic demands of growth are at their highest. Interestingly, growth rate was not influenced by ALAN. This suggests that either the negative physiological impacts of ALAN may be concealed when food is provided ad libitum, the observed changes in digestive efficiency were too small to affect growth or condition, or that ALAN-exposed birds had reduced energy expenditure. Our results illustrate that the health impacts of ALAN on wild animals should not be restricted to traditional markers like body mass or growth rate, but instead on a wide array of integrated physiological traits.

Short communication: Levels of land use and land cover in Phoenix, Arizona are associated with elevated plasma triglycerides in the Gambel's Quail, Callipepla gambelii.

Gambel's Quail, Callipepla gambelii, are gregarious birds commonly found in the southwestern deserts of the United States and Northwestern Mexico. With expanding urbanization, these birds are often found in exurban and suburban areas where they have access to food sources that may differ from those used by birds living in rural habitats and, as a result, also differ morphologically and physiologically. To investigate this hypothesis, we compared the morphology and nutritional physiology of quail sampled at sites varying with respect to land use and cover. We hypothesized that quail living in more developed areas have access to a greater variety of and to more stable food resources, and predicted that morphology and nutritional physiology would be associated with degree of urbanization. We sampled adult birds at locations in the greater Phoenix metropolitan, Arizona (USA) area that vary with respect to land use and cover types. At the time of capture, birds were weighed and chest circumference was recorded. We also collected a blood sample from the jugular vein of each individual for analysis of plasma glucose, total proteins, triglycerides, and free glycerol. Consistent with the hypothesis, birds living in more developed environments had larger chest circumferences and higher circulating lipid concentrations than birds living in less developed areas, suggesting greater access to lipid-rich foods. In addition, the areal proportion of grass and lakes was negatively correlated to plasma free glycerol (r = -0.46, p = .031), and positively, but not significantly, correlated to plasma protein concentrations (r = 0.388, p = .073). These results suggest that quail living in areas with more grass have access to less dietary fats than urban birds. The findings are the first to indicate an association between urbanization and the morphology and nutritional physiology of Gambel's Quail, but further study using more and larger samples is needed before these findings can be generalized.

Exposure to artificial light at night increases innate immune activity during development in a precocial bird.

Humans have greatly altered Earth's night-time photic environment via the production of artificial light at night (ALAN; e.g. street lights, car traffic, billboards, lit buildings). ALAN is a problem of growing importance because it may significantly disrupt the seasonal and daily physiological rhythms and behaviors of animals. There has been considerable interest in the impacts of ALAN on health of humans and other animals, but most of this work has centered on adults and we know comparatively little about effects on young animals. We exposed 3-week-old king quail (Excalfactoria chinensis) to a constant overnight blue-light regime for 6 weeks and assessed weekly bactericidal activity of plasma against Escherichia coli - a commonly employed metric of innate immunity in animals. We found that chronic ALAN exposure significantly increased bactericidal activity and that this elevation in immune performance manifested at different developmental time points in males and females. Whether this short-term increase in immune activity can be extended to wild animals, and whether ALAN-mediated increases in immune activity have positive or negative fitness effects, are unknown and will provide interesting avenues for future studies.

Carotenoid coloration is related to fat digestion efficiency in a wild bird.

Some of the most spectacular visual signals found in the animal kingdom are based on dietarily derived carotenoid pigments (which cannot be produced de novo), with a general assumption that carotenoids are limited resources for wild organisms, causing trade-offs in allocation of carotenoids to different physiological functions and ornamentation. This resource trade-off view has been recently questioned, since the efficiency of carotenoid processing may relax the trade-off between allocation toward condition or ornamentation. This hypothesis has so far received little exploratory support, since studies of digestive efficiency of wild animals are limited due to methodological difficulties. Recently, a method for quantifying the percentage of fat in fecal samples to measure digestive efficiency has been developed in birds. Here, we use this method to test if the intensity of the carotenoid-based coloration predicts digestive efficiency in a wild bird, the house finch (Haemorhous mexicanus). The redness of carotenoid feather coloration (hue) positively predicted digestion efficiency, with redder birds being more efficient at absorbing fats from seeds. We show for the first time in a wild species that digestive efficiency predicts ornamental coloration. Though not conclusive due to the correlative nature of our study, these results strongly suggest that fat extraction might be a crucial but overlooked process behind many ornamental traits.

Negative energy balance in a male songbird, the Abert's towhee, constrains the testicular endocrine response to luteinizing hormone stimulation.

Energy deficiency can suppress reproductive function in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary-gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none have investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone responsiveness of the HPG axis. Wild-caught birds were either ad libitum fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma testosterone response to GnRH challenge. Energy deficiency did, however, decrease the plasma testosterone responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting of a decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity.

Negative energy balance in a male songbird, the Abert's Towhee, constrains the testicular endocrine response to luteinizing hormone stimulation.

Energy deficiency can suppress reproductive functions in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary-gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none has investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's Towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone (T) responsiveness of the HPG axis. Wild-caught birds were either ad libitum-fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma T response to GnRH challenge. Energy deficiency did, however, decrease the plasma T responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting in decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity.

Urban house finches are more resistant to the effects of artificial light at night.

Rapid urbanization of habitats alters the physical, chemical, auditory, and photic environments of human and wild animal inhabitants. One of the most widespread transformations is caused by artificial light at night (ALAN), but it is not clear the extent to which individuals acclimate to such rapid environmental change. Here, we tested the hypothesis that urban birds show increased resistance to harmful behavioral, parasitological, and physiological effects of ALAN. We captured house finches (Haemorhous mexicanus), a bird that commonly inhabits cities and their natural surroundings, from two urban and two rural sites in Phoenix, Arizona, USA, which differ by both degree of urbanization and by multiple orders of magnitude in ALAN intensity, and placed them in a common garden laboratory setting. We exposed half of the birds from each habitat type to ecologically relevant levels of night lighting during the subjective night and found that, while ALAN exposure reduced sleep in both urban and rural birds, ALAN-exposed urban birds were able to sleep longer than ALAN-exposed rural birds. We also found that ALAN exposure increased the proliferation rate of an intestinal coccidian parasite (Isospora spp.) in both urban and rural birds, but that the rate of proliferation was lower in urban relative to rural birds. We found that night lighting suppressed titers of feather corticosterone in rural but not urban birds, suggesting that light impairs HPA function through chronic stress or suppression of its circadian rhythmicity, and that urban birds were again resistant to this effect. Mediation analyses show that the effect of ALAN exposure in rural birds was significantly sleep-mediated for feather corticosterone but not coccidiosis, suggesting a diversity of mechanisms by which ALAN alters physiology. We contribute further evidence that animals from night-lit habitats can develop resistance to ALAN and its detrimental effects.

Bird-feeder cleaning lowers disease severity in rural but not urban birds.

Animals inhabiting urban areas often experience elevated disease threats, putatively due to factors such as increased population density and horizontal transmission or decreased immunity (e.g. due to nutrition, pollution, stress). However, for animals that take advantage of human food subsidies, like feeder-visiting birds, an additional mechanism may include exposure to contaminated feeders as fomites. There are some published associations between bird feeder presence/density and avian disease, but to date no experimental study has tested the hypothesis that feeder contamination can directly impact disease status of visiting birds, especially in relation to the population of origin (i.e. urban v. rural, where feeder use/densities naturally vary dramatically). Here we used a field, feeder-cleaning experimental design to show that rural, but not urban, house finches (Haemorhous mexicanus) showed increased infection from a common coccidian endoparasite (Isospora spp.) when feeders were left uncleaned and that daily cleaning (with diluted bleach solution) over a 5-week period successfully decreased parasite burden. Moreover, this pattern in rural finches was true for males but not females. These experimental results reveal habitat- and sex-specific harmful effects of bird feeder use (i.e. when uncleaned in rural areas). Our study is the first to directly indicate to humans who maintain feeders for granivorous birds that routine cleaning can be critical for ensuring the health and viability of visiting avian species.

A New Framework for Urban Ecology: An Integration of Proximate and Ultimate Responses to Anthropogenic Change.

As urban areas continue to grow, understanding how species respond and adapt to urban habitats is becoming increasingly important. Knowledge of the mechanisms behind observed phenotypic changes of urban-dwelling animals will enable us to better evaluate the impact of urbanization on current and future generations of wildlife and predict how animals respond to novel environments. Recently, urban ecology has emerged not only as a means of understanding organismal adaptation but also as a framework for exploring mechanisms mediating evolutionary phenomena. Here, we have identified four important research topics that will advance the field of urban ecology and shed light on the proximate and ultimate causes of the phenotypic differences commonly seen among species and populations that vary in their responses to urbanization. First, we address the ecological and socio-economic factors that characterize cities, how they might interact with each other, and how they affect urban species. Second, we ask which are the proximate mechanisms underlying the emergence over time of novel traits in urban organisms, focusing on developmental effects. Third, we emphasize the importance of understanding the ultimate causations that link phenotypic shifts to function. This question highlights the need to quantify the strength and direction of selection that urban individuals are exposed to, and whether the phenotypic shifts associated with life in the city are adaptive. Lastly, we stress the need to translate how individual-level responses scale up to population dynamics. Understanding the mechanistic underpinnings of variation among populations and species in their responses to urbanization will unravel species resilience to environmental perturbation, which will facilitate predictive models for sustainability and development of green cities that maintain or even increase urban biodiversity and wildlife health and wellbeing.

No Effect of Human Presence at Night on Disease, Body Mass, or Metabolism in Rural and Urban House Finches (Haemorhous mexicanus).

Global urban development continues to accelerate and have diverse effects on wildlife. Although most studies of anthropogenic impacts on animals have focused on indirect effects (e.g., environmental modifications like habitat change or pollution), there may also be direct effects of physical human presence and actions on wildlife stress, behavior, and persistence in cities. Most studies on how humans physically interact with wildlife have focused on the active, daytime phase of diurnal animals, rarely considering effects of our night-time activities. We hypothesized that, if night-time human presence is a stressor for wildlife that are not commonly exposed to humans, night-disturbed rural animals would show stronger physiological signs of elevated stress than would urban individuals. Specifically, we experimentally investigated the effects of human presence at night (HPAN) on disease, body mass, and mass-specific metabolic rates in urban- and rural-caught house finches (Haemorhous mexicanus) in captivity. Our HPAN treatment consisted of a human entering the housing room of the birds and briefly jostling the home cages of each finch as the person walked around the room for a 3-min period on five randomly selected nights per week. Compared with a control (night-undisturbed) group, we found that HPAN greatly increased the odds finches were awake for ca. 33 min post-disturbance, but that chronic treatment did not alter body mass, parasitic infection by coccidian endoparasites, or mass-specific basal metabolic rates. Additionally, finches caught from urban and rural sites did not differ in their response to the treatment. Overall, our results are consistent with those showing that brief but regular human disturbances can have acute negative effects on wildlife, but carry few if any long-term metabolic or disease-related costs in fast-lived birds. However, these findings contrast with the broad, chronic physiological effects of other anthropogenic changes, such as artificial light at night, and highlight the differential impacts that various human activities (which differ in sensory stimulus type, perceived threat, duration and intensity, etc.) can have on wildlife health and behavior.

Plumage micro-organisms and preen gland size in an urbanizing context.

Urbanization of Earth's habitats has led to considerable loss of biodiversity, but the driving ecological mechanism(s) are not always clear. Vertebrates like birds typically experience urban alterations to diet, habitat availability, and levels of predation or competition, but may also be exposed to greater or more pathogenic communities of microbes. Birds have been popular subjects of urban ecological research but, to our knowledge, no study has assessed how urban conditions influence the microbial communities on bird plumage. Birds carry a large variety of microorganisms on their plumage and some of them have the capacity to degrade feather keratin and alter plumage integrity. To limit the negative effects of these feather-degrading bacteria, birds coat their feathers with preen gland secretions containing antibacterial substances. Here we examined urban-rural variation in feather microbial abundance and preen gland size in house finches (Haemorhous mexicanus). We found that, although urban and rural finches carry similar total-cultivable microbial loads on their plumage, the abundance of feather-degrading bacteria was on average three times higher on the plumage of urban birds. We also found an increase in preen gland size along the gradient of urbanization, suggesting that urban birds may coat their feathers with more preen oil to limit the growth or activity of feather-degrading microbes. Given that greater investment in preening is traded-off against other immunological defenses and that feather-degrading bacteria can alter key processes like thermoregulation, aerodynamics, and coloration, our findings highlight the importance of plumage microbes and microbial defenses on the ecology of urban birds.

Urban-Rural Differences in Eye, Bill, and Skull Allometry in House Finches (Haemorhous mexicanus).

Allometry, the proportional scaling of log trait size with log body size, evolves to optimize allocation to growth of separate structures and is a major constraint on the functional limits of animal traits. While there are many studies demonstrating the rigidity of allometry across traits and taxa, comparatively less work has been done on allometric variation across environments within species. Rapidly changing environments, such as cities, may be prime systems for studying the flexibility of allometry because they uniquely alter many environmental parameters (e.g., habitat, light, noise). We studied size variation, allometry, and allometric dispersion of craniofacial traits in both sexes of urban and rural house finches (Haemorhous mexicanus) because many traits in the head are ecologically critical to the survival and acclimation of birds to their environment (e.g., brain: response to cognitive challenges; bill: foraging modes). We found that urban finches had shorter eye axial lengths and skull widths, but longer (but not wider or deeper) bills, than rural finches. Also, allometric slopes of eye, skull, and bill traits differed based on sex and environment. In the rural environment, females had a far steeper allometric slope for eye axial length than males, but such slopes were similar between males and females in the city. Skull allometry was similar for males and females in both environments, but urban birds had a shallower slope for skull length (but not width) than rural birds. Other traits only differed by sex (males had a steeper slope for bill width), and one trait did not differ based on either sex or environment (bill depth). The dispersion of points around the allometric line did not differ by sex or environment for any craniofacial variable. Due to the significant but low genetic divergence between urban and rural finch populations, allometric differences are probably largely driven by plastic forces. We suggest that differences in diet and cognitive demand of urban environments may drive these allometric patterns. Overall, these results indicate that allometry may shift due to rapid environmental change and differentially so between the sexes.