Acute stress and restricted diet reduce bill-mediated heat dissipation in the song sparrow (Melospiza melodia): implications for optimal thermoregulation.

We used thermal imaging to show that two environmental factors - acute stress and diet - influence thermoregulatory performance of a known thermal window, the avian bill. The bill plays important roles in thermoregulation and water balance. Given that heat loss through the bill is adjustable through vasoconstriction and vasodilation, and acute stress can cause vasoconstriction in peripheral body surfaces, we hypothesized that stress may influence the bill's role as a thermal window. We further hypothesized that diet influences heat dissipation from the bill, given that body condition influences the surface temperature of another body region (the eye region). We measured the surface temperature of the bills of song sparrows (Melospiza melodia) before, during and after handling by an observer at 37°C ambient temperature. We fed five birds a restricted diet intended to maintain body mass typical of wild birds, and we fed six birds an unrestricted diet for 5 months prior to experiments. Acute stress caused a decrease in the surface temperature of the bill, resulting in a 32.4% decrease in heat dissipation immediately following acute stress, before recovering over approximately 2.3 min. The initial reduction and subsequent recovery provide partial support for the hemoprotective and thermoprotective hypotheses, which predict a reduction or increase in peripheral blood flow, respectively. Birds with unrestricted diets had larger bills and dissipated more heat, indicating that diet and body condition influence bill-mediated heat dissipation and thermoregulation. These results indicate that stress-induced vascular changes and diet can influence mechanisms of heat loss and potentially inhibit optimal thermoregulation.

Novel approaches for assessing acclimatization in birds reveal seasonal changes in peripheral heat exchange and thermoregulatory behaviors.

Using thermography and behavioral analyses, we found that heat exchange and thermoregulatory behaviors changed seasonally in chipping sparrows (Spizella passerina). Studies on seasonal acclimatization in birds have primarily involved metabolic measurements, few of which have investigated behaviors, and none have investigated changes in peripheral heat exchange. We captured chipping sparrows in the winter and summer of 2022 in Wilmington, North Carolina, USA, and we collected thermal images of these birds at 15.0, 27.5 and 40.0°C. We found that heat dissipation through the bill and legs changed seasonally, but surprisingly both were higher in winter than in summer. We found that heat dissipating behaviors were more common in winter, whereas heat conserving behaviors were more common in summer, and that behaviors associated with resource costs (e.g. panting) or predation risk (e.g. bill tucking) showed the most distinct differences between seasons. Meanwhile, low-cost and low-risk postural adjustments (e.g. feather adjustments and tarsus exposure) did not vary as strongly between seasons but followed similar trends. The seasonal adjustments to behaviors suggest that non-acclimatized birds must use costly thermoregulatory behaviors more frequently than acclimatized birds. The use of thermography resulted in the discovery of one completely novel behavior, and the first detection of a known behavior in a new species. Both novel behaviors aided in evaporative heat loss and occurred more commonly in winter, supporting the presence of seasonal acclimatization as evidenced by behavioral adjustments. These results provide novel insights into the process of acclimatization and suggest a role for behavioral adjustments in seasonal acclimatization.

Activity analysis of thermal imaging videos using a difference imaging approach.

Infrared thermal imaging is a passive imaging technique that captures the emitted radiation from an object to estimate surface temperature, often for inference of heat transfer. Infrared thermal imaging offers the potential to detect movement without the challenges of glare, shadows, or changes in lighting associated with visual digital imaging or active infrared imaging. In this paper, we employ a frame subtraction algorithm for extracting the pixel-by-pixel relative change in signal from a fixed focus video file, tailored for use with thermal imaging videos. By summing the absolute differences across an entire video, we are able to assign quantitative activity assessments to thermal imaging data for comparison with simultaneous recordings of metabolic rates. We tested the accuracy and limits of this approach by analyzing movement of a metronome and provide an example application of the approach to a study of Darwin's finches. In principle, this "Difference Imaging Thermography" (DIT) would allow for activity data to be standardized to energetic measurements and could be applied to any radiometric imaging system.

Husbandry of wild-caught song sparrows (Melospiza melodia).

Conservation and research efforts occasionally rely upon bringing wild animals into human care to establish breeding programs and to understand their biology. Wild-caught birds may have husbandry requirements that differ from captive-reared animals due, in part, to their social development in the wild and potential exposure to novel pathogens. We developed husbandry techniques to minimize stress and monitor health in a population of wild-caught song sparrows (Melospiza melodia). We describe enclosure conditions, diet and enrichment, and best practices for stress reduction. In addition, we describe several health monitoring strategies, including assessing feces quality, body condition scores, and specific signs of infection. These techniques led to successful housing of song sparrows during formal behavioral and developmental studies. This information will be useful for guiding the husbandry of wild-caught passerine birds in the future.

Experimental support for food limitation of a short-distance migratory bird wintering in the temperate zone.

The Winter Food Limitation Hypothesis (WFLH) states that winter food abundance is a dominant source of population limitation of migratory birds. Evidence is accumulating that long-distance migratory birds wintering in tropical climates have high overwinter survival probabilities and that winter food limitation mainly affects their fitness nonlethally by limiting energetic reserves necessary for successful reproduction. In contrast, the relative roles of direct mortality vs. indirect effects caused by food limitation have not been investigated thoroughly on short-distance migratory birds wintering in temperate zones, where they face thermal challenges. We performed the first test of the WFLH for a temperate migratory bird in the wild on the Swamp Sparrow (Melospiza georgiana), with a replicated plot-wide food supplementation experiment. In contrast to tropical, but consistent with other temperate-wintering migrants, Swamp Sparrows on unmanipulated plots showed relatively low apparent survival across the winter. Following food addition, birds (1) immigrated to experimental plots, which subsequently supported approximately 50% higher abundances, (2) experienced increases of within-season apparent survival of 8-10%, depending on age/sex class, and (3) had higher-scaled mass index values, all supporting winter food limitation. The last two findings are interrelated because birds with higher scaled mass had higher survival probabilities, further supporting direct effects of winter food limitation. Food limitation of fat reserves might also have indirect effects on reproductive success by limiting migration timing and survival during migration. Increases in scaled mass were higher in females, suggesting that they are disproportionately affected by food limitation, possibly through competition. Based on Robust Design Modeling, we found no support for emigration prior to food addition, indicating that our estimates of mortality are unbiased.

Climate, ecological release and bill dimorphism in an island songbird.

Sexual size dimorphism is expected to be more pronounced in vertebrates on islands, particularly in trophic characters, as a response to decreased interspecific competition for food. We found (based on measurements of 1423 museum specimens) that bill size dimorphism was greater in island than mainland populations of song sparrows. However, dimorphism varied among islands and was positively correlated with high summer temperature and island size. Island song sparrow bills follow the overall positive temperature bill size relationship for California song sparrows, which includes larger bills on large, warmer islands. Large bills dissipate more heat and may be an adaptation to summer heat stress. Dimorphism increases because the slope for males is greater than females. Thus, the greater magnitude of bill dimorphism on islands with warmer summers may result from males experiencing greater thermal stress during territorial activity, creating different thermal optima. In contrast, bill dimorphism was unrelated to climate on the mainland. We hypothesize that reduced interspecific competition releases island populations from a constraint so that sex-specific physiological optima can be achieved, whereas mainland birds are constrained.

Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence.

In addition to the observed high diversity of species in the tropics, divergence among populations of the same species exists over short geographic distances in both phenotypic traits and neutral genetic markers. Divergence among populations suggests great potential for the evolution of reproductive isolation and eventual speciation. In birds, song can evolve quickly through cultural transmission and result in regional dialects, which can be a critical component of reproductive isolation through variation in female preference. We examined female and male behavioral responses to local and nonlocal dialects in two allopatric populations of rufous-collared sparrows (Zonotrichia capensis) in the Andes Mountains of Ecuador. Here we show that female sparrows prefer their natal song dialect to the dialect of an allopatric population that is just 25 km away and separated by an unsuitable higher-elevation habitat (pass of 4,200 m), thus providing evidence of prezygotic reproductive isolation among populations. Males showed similar territorial responses to all conspecific dialects with no consistent difference with respect to distance, making male territoriality uninformative for estimating reproductive isolation. This study provides novel evidence for culturally based prezygotic isolation over very short distances in a tropical bird.

Simulated heat waves reduce cognitive and motor performance of an endotherm.

Heat waves cause mass mortality of animals, including humans, across the globe annually, which has drawn new attention to how animals cope with high air temperatures. Recent field research has explored behavioral responses to high air temperatures, which can influence reproductive success and mortality.Less well studied are the effects of high air temperatures on cognition, which may underlie behavioral changes. Specifically, it is poorly known if cognitive declines occur at high temperatures, and if cognitive and motor components of behavior are similarly affected.We tested how well zebra finches (Taeniopygia guttata castanotis), a model for cognition research, performed two learned foraging tasks (color association and detour-reaching) at mild (22°C) and high (43 and 44°C) air temperatures that occur naturally in their range. We habituated birds to the trial conditions and temperatures on days preceding the test trials and at the trial temperature for 30 min immediately prior to each test trial. Trials lasted less than 10 min. At high air temperatures, zebra finches exhibited heat dissipation behaviors during most tasks, suggesting thermoregulatory challenge.Cognitive performance declined at high air temperatures in two of three measures: Color association was unaffected, but birds missed more food rewards, and did more unproductive behaviors. Motor performance declined at high temperatures on the color association task, including longer times to complete the task, move between food rewards, and process individual seeds. Performance declines varied among components of behavior and among individuals.We combined our behavioral data with existing climate data and predicted that in the austral summer of 2018-2019, zebra finches experienced air temperatures that caused cognitive and motor declines in our captive birds in 34% and 45% of their Australian range, respectively.This study provides novel experimental evidence that high air temperatures cause cognitive and motor performance decline in birds. Further, our results provide insights to how those declines might affect bird ecology and evolution. First, differences in declines among behavioral components may allow identification of behaviors that are most susceptible to decline in the wild. Second, variation in performance declines and heat dissipation behaviors among individuals suggests variability in heat tolerance, which could lead to differential fitness in the wild. Last, these results suggest that high air temperatures cause cognitive declines in the wild and that understanding cognition could help refine predictive models of population persistence.

Evidence of feline immunodeficiency virus, feline leukemia virus, and Toxoplasma gondii in feral cats on Mauna Kea, Hawaii.

We determined prevalence to feline immunodeficiency virus (FIV) antibodies, feline leukemia virus (FeLV) antigen, and Toxoplasma gondii antibodies in feral cats (Felis catus) on Mauna Kea Hawaii from April 2002 to May 2004. Six of 68 (8.8%) and 11 of 68 (16.2%) cats were antibody positive to FIV and antigen positive for FeLV, respectively; 25 of 67 (37.3%) cats were seropositive to T. gondii. Antibodies to FeLV and T. gondii occurred in all age and sex classes, but FIV occurred only in adult males. Evidence of current or previous infections with two of these infectious agents was detected in eight of 64 cats (12.5%). Despite exposure to these infectious agents, feral cats remain abundant throughout the Hawaiian Islands.

White-crowned sparrow males show immediate flexibility in song amplitude but not in song minimum frequency in response to changes in noise levels in the field.

The soundscape acts as a selective agent on organisms that use acoustic signals to communicate. A number of studies document variation in structure, amplitude, or timing of signal production in correspondence with environmental noise levels thus supporting the hypothesis that organisms are changing their signaling behaviors to avoid masking. The time scale at which organisms respond is of particular interest. Signal structure may evolve across generations through processes such as cultural or genetic transmission. Individuals may also change their behavior during development (ontogenetic change) or in real time (i.e., immediate flexibility). These are not mutually exclusive mechanisms, and all must be investigated to understand how organisms respond to selection pressures from the soundscape. Previous work on white-crowned sparrows (Zonotrichia leucophrys) found that males holding territories in louder areas tend to sing higher frequency songs and that both noise levels and song frequency have increased over time (30 years) in urban areas. These previous findings suggest that songs are changing across generations; however, it is not known if this species also exhibits immediate flexibility. Here, we conducted an exploratory, observational study to ask whether males change the minimum frequency of their song in response to immediate changes in noise levels. We also ask whether males sing louder, as increased minimum frequency may be physiologically linked to producing sound at higher amplitudes, in response to immediate changes in environmental noise. We found that territorial males adjust song amplitude but not minimum frequency in response to changes in environmental noise levels. Our results suggest that males do not show immediate flexibility in song minimum frequency, although experimental manipulations are needed to test this hypothesis further. Our work highlights the need to investigate multiple mechanisms of adaptive response to soundscapes.

Patterns of Song across Natural and Anthropogenic Soundscapes Suggest That White-Crowned Sparrows Minimize Acoustic Masking and Maximize Signal Content.

Soundscapes pose both evolutionarily recent and long-standing sources of selection on acoustic communication. We currently know more about the impact of evolutionarily recent human-generated noise on communication than we do about how natural sounds such as pounding surf have shaped communication signals over evolutionary time. Based on signal detection theory, we hypothesized that acoustic phenotypes will vary with both anthropogenic and natural background noise levels and that similar mechanisms of cultural evolution and/or behavioral flexibility may underlie this variation. We studied song characteristics of white-crowned sparrows (Zonotrichia leucophrys nuttalli) across a noise gradient that includes both anthropogenic and natural sources of noise in San Francisco and Marin counties, California, USA. Both anthropogenic and natural soundscapes contain high amplitude low frequency noise (traffic or surf, respectively), so we predicted that birds would produce songs with higher minimum frequencies in areas with higher amplitude background noise to avoid auditory masking. We also anticipated that song minimum frequencies would be higher than the projected lower frequency limit of hearing based on site-specific masking profiles. Background noise was a strong predictor of song minimum frequency, both within a local noise gradient of three urban sites with the same song dialect and cultural evolutionary history, and across the regional noise gradient, which encompasses 11 urban and rural sites, several dialects, and several anthropogenic and natural sources of noise. Among rural sites alone, background noise tended to predict song minimum frequency, indicating that urban sites were not solely responsible for driving the regional pattern. These findings support the hypothesis that songs vary with local and regional soundscapes regardless of the source of noise. Song minimum frequency from five core study sites was also higher than the lower frequency limit of hearing at each site, further supporting the hypothesis that songs vary to transmit through noise in local soundscapes. Minimum frequencies leveled off at noisier sites, suggesting that minimum frequencies are constrained to an upper limit, possibly to retain the information content of wider bandwidths. We found evidence that site noise was a better predictor of song minimum frequency than territory noise in both anthropogenic and natural soundscapes, suggesting that cultural evolution rather than immediate behavioral flexibility is responsible for local song variation. Taken together, these results indicate that soundscapes shape song phenotype across both evolutionarily recent and long-standing soundscapes.

Seasonal dimorphism in the horny bills of sparrows.

Bill size is often viewed as a species-specific adaptation for feeding, but it sometimes varies between sexes, suggesting that sexual selection or intersexual competition may also be important. Hypotheses to explain sexual dimorphism in avian bill size include divergence in feeding niche or thermoregulatory demands, intrasexual selection based on increased competition among males, or female preference. Birds also show seasonal changes in bill size due to shifts in the balance between growth rate and wear, which may be due to diet or endogenous rhythms in growth. Insight into the function of dimorphism can be gained using the novel approach of digital x-ray imaging of museum skins to examine the degree to which the skeletal core or the rhamphotheca contribute to overall dimorphism. The rhamphotheca is ever-growing and ever-wearing, varying in size throughout life; whereas the skeletal core shows determinant growth. Because tidal marsh sparrows are more dimorphic in bill size than related taxa, we selected two marsh taxa to investigate dimorphism and seasonality in the size of the overall bill, the skeletal core, and the rhamphotheca. Bill size varied by sex and season, with males having larger bills than females, and bill size increasing from nonbreeding to breeding season more in males. Skeletal bill size varied with season, but not sex. The rhamphotheca varied primarily with sex; males had a larger rhamphotheca (corrected for skeletal bill size), which showed a greater seasonal increase than females. The rhamphotheca, rather than the skeletal bill, was responsible for sexual dimorphism in overall bill size, which was particularly well developed in the breeding season. The size of the rhamphotheca may be a condition-based character that is shaped by sexual selection. These results are consistent with the evidence that bill size is influenced by sexual selection as well as trophic ecology.

The influence of the California marine layer on bill size in a generalist songbird.

The hypothesis is tested that birds in hotter and drier environments may have larger bills to increase the surface area for heat dissipation. California provides a climatic gradient to test the influence of climate on bill size. Much of California experiences dry warm/hot summers and coastal areas experience cooler summers than interior localities. Based on measurements from 1488 museum skins, song sparrows showed increasing body-size-corrected bill surface area from the coast to the interior and declining in the far eastern desert. As predicted by Newton's convective heat transfer equation, relative bill size increased monotonically with temperature, and then decreased where average high temperatures exceed body temperature. Of the variables considered, distance from coast, average high summer temperature, and potential evapotranspiration showed a strong quadratic association with bill size and rainfall had a weaker negative relationship. Song sparrows on larger, warmer islands also had larger bills. A subsample of radiographed specimens showed that skeletal bill size is also correlated with temperature, demonstrating that bill size differences are not a result of variation in growth and wear of keratin. Combined with recent thermographic studies of heat loss in song sparrow bills, these results support the hypothesis that bill size in California song sparrows is selected for heat dissipation.

Heat loss may explain bill size differences between birds occupying different habitats.

BACKGROUND: Research on variation in bill morphology has focused on the role of diet. Bills have other functions, however, including a role in heat and water balance. The role of the bill in heat loss may be particularly important in birds where water is limiting. Song sparrows localized in coastal dunes and salt marsh edge (Melospiza melodia atlantica) are similar in size to, but have bills with a 17% greater surface area than, those that live in mesic habitats (M. m. melodia), a pattern shared with other coastal sparrows. We tested the hypotheses that sparrows can use their bills to dissipate "dry" heat, and that heat loss from the bill is higher in M. m. atlantica than M. m. melodia, which would indicate a role of heat loss and water conservation in selection for bill size. METHODOLOGY/PRINCIPAL FINDINGS: Bill, tarsus, and body surface temperatures were measured using thermal imaging of sparrows exposed to temperatures from 15-37°C and combined with surface area and physical modeling to estimate the contribution of each body part to total heat loss. Song sparrow bills averaged 5-10°C hotter than ambient. The bill of M. m atlantica dissipated up to 33% more heat and 38% greater proportion of total heat than that of M. m. melodia. This could potentially reduce water loss requirements by approximately 7.7%. CONCLUSIONS/SIGNIFICANCE: This >30% higher heat loss in the bill of M. m. atlantica is independent of evaporative water loss and thus could play an important role in the water balance of sparrows occupying the hot and exposed dune/salt marsh environments during the summer. Heat loss capacity and water conservation could play an important role in the selection for bill size differences between bird populations and should be considered along with trophic adaptations when studying variation in bill size.