Diet and the evolution of ADH7 across seven orders of mammals.

Dietary variation within and across species drives the eco-evolutionary responsiveness of genes necessary to metabolize nutrients and other components. Recent evidence from humans and other mammals suggests that sugar-rich diets of floral nectar and ripe fruit have favoured mutations in, and functional preservation of, the ADH7 gene, which encodes the ADH class 4 enzyme responsible for metabolizing ethanol. Here we interrogate a large, comparative dataset of ADH7 gene sequence variation, including that underlying the amino acid residue located at the key site (294) that regulates the affinity of ADH7 for ethanol. Our analyses span 171 mammal species, including 59 newly sequenced. We report extensive variation, especially among frugivorous and nectarivorous bats, with potential for functional impact. We also report widespread variation in the retention and probable pseudogenization of ADH7. However, we find little statistical evidence of an overarching impact of dietary behaviour on putative ADH7 function or presence of derived alleles at site 294 across mammals, which suggests that the evolution of ADH7 is shaped by complex factors. Our study reports extensive new diversity in a gene of longstanding ecological interest, offers new sources of variation to be explored in functional assays in future study, and advances our understanding of the processes of molecular evolution.

Metals and metalloids in nestling tree swallows and their dietary items near oilsands mine operations in Northern Alberta.

Tree swallows (Tachycineta bicolor) nesting near oilsands development in northern Alberta are potentially exposed to elevated levels of metals. The objective of this study was to determine whether levels of metals and metalloid elements in dietary items and tissues of nestling tree swallows inhabiting areas near oilsands mine operations were higher compared to those of reference sites. We hypothesized that if there was increased, industry-related exposure to metals, it would be via the diet. We identified the invertebrate prey in the stomach contents of nestlings. We also collected invertebrates using Malaise traps near nest boxes, and analyzed those taxa found in the nestling diet to understand potential variability in metal exposure. For most elements, we found no significant differences in concentrations in the liver, kidney, or stomach contents between sites near to and far from oilsands operations. Concentrations of five elements were positively correlated among tissues and stomach contents. For invertebrates collected from Malaise traps, location differences occurred in some absolute elemental concentrations, which were most often highest at reference sites away from mining operations. We found no evidence that nestling tree swallows accumulated metals approaching toxic levels. Tree swallows consumed relatively high quantities of terrestrial insects, possibly limiting exposure to water borne, food-web-related contaminants. We suggest that annual variability associated with elemental exposure and dietary levels of elements be considered when interpreting concentrations in bird tissues.

The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability.

Variation in prey resources influences the diet and behaviour of predators. When prey become limiting, predators may travel farther to find preferred food or adjust to existing local resources. When predators are habitat limited, local resource abundance impacts foraging success. We analysed the diet of Myotis lucifugus (little brown bats) from Nova Scotia (eastern Canada) to the Northwest Territories (north-western Canada). This distribution includes extremes of season length and temperature and encompasses colonies on rural monoculture farms, and in urban and unmodified areas. We recognized nearly 600 distinct species of prey, of which ≈30% could be identified using reference sequence libraries. We found a higher than expected use of lepidopterans, which comprised a range of dietary richness from ≈35% early in the summer to ≈55% by late summer. Diptera were the second largest prey group consumed, representing ≈45% of dietary diversity early in the summer. We observed extreme local dietary variability and variation among seasons and years. Based on the species of insects that were consumed, we observed that two locations support prey species with extremely low pollution and acidification tolerances, suggesting that these are areas without environmental contamination. We conclude that there is significant local population variability in little brown bat diet that is likely driven by seasonal and geographical changes in insect diversity, and that this prey may be a good indicator of environment quality.

Evidence of late-summer mating readiness and early sexual maturation in migratory tree-roosting bats found dead at wind turbines.

Understanding animal mating systems is an important component of their conservation, yet the precise mating times for many species of bats are unknown. The aim of this study was to better understand the details and timing of reproductive events in species of bats that die most frequently at wind turbines in North America, because such information can help inform conservation strategies. We examined the reproductive anatomy of hoary bats (Lasiurus cinereus), eastern red bats (L. borealis), and silver-haired bats (Lasionycteris noctivagans) found dead beneath industrial-scale wind turbines to learn more about when they mate. We evaluated 103 L. cinereus, 18 L. borealis, and 47 Ln. noctivagans from wind energy facilities in the United States and Canada. Histological analysis revealed that most male L. cinereus and L. borealis, as well as over half the Ln. noctivagans examined had sperm in the caudae epididymides by late August, indicating readiness to mate. Testes regression in male hoary bats coincided with enlargement of seminal vesicles and apparent growth of keratinized spines on the glans penis. Seasonality of these processes also suggests that mating could occur during August in L. cinereus. Spermatozoa were found in the uterus of an adult female hoary bat collected in September, but not in any other females. Ovaries of all females sampled had growing secondary or tertiary follicles, indicating sexual maturity even in first-year females. Lasiurus cinereus, L. borealis, and Ln. noctivagans are the only North American temperate bats in which most first-year young of both sexes are known to sexually mature in their first autumn. Our findings provide the first detailed information published on the seasonal timing of mating readiness in these species most affected by wind turbines.

Variable variation: annual and seasonal changes in offspring sex ratio in a bat.

Many organisms produce offspring with sex-ratios that deviate from equal numbers of males and females, and numerous adaptive explanations have been proposed. In some species, offspring sex-ratio varies across the reproductive season, again with several explanations as to why this might be adaptive. However, patterns for birds and mammals are inconsistent, and multiple factors are likely involved. Long-term studies on a variety of species may help untangle the complexity. I analyzed a long-term data set on the variation in offspring sex-ratio of the big brown bat, Eptesicus fuscus, a temperate-zone, insectivorous species. Sex ratio varied seasonally, but only in some years. Births early in the season were significantly female biased in years in which parturition occurred relatively early, but not in years with late parturition. Survival of female pups increased with earlier median birth date for the colony, and early-born females were more likely to survive and reproduce as one-year olds, compared to later-born pups. I argue that, due to the unusual timing of reproductive activities in male and female bats that hibernate, producing female offspring early in the year increases their probability of reproducing as one year olds, but this is not the case for male offspring. Thus, mothers that can give birth early in the year, benefit most by producing a female pup. The relative benefit of producing female or male offspring varies depending on the length of the growing season and thus the time available for female pups to reach sexual maturity. This suggests that not only does sex-ratio vary seasonally and among years, depending on the condition of the mother and the environment, but also likely varies geographically due to differences in season length.

Influence of urbanization on demography of little brown bats (Myotis lucifugus) in the prairies of North America.

BACKGROUND: We address three key gaps in research on urban wildlife ecology: insufficient attention to (1) grassland biomes, (2) individual- and population-level effects, and (3) vertebrates other than birds. We hypothesized that urbanization in the North American Prairies, by increasing habitat complexity (via the proliferation of vertical structures such as trees and buildings), thereby enhancing the availability of day-roosts, tree cover, and insects, would benefit synanthropic bats, resulting in increased fitness among urban individuals. METHODOLOGY/PRINCIPAL FINDINGS: Over three years, we captured more than 1,600 little brown bats (Myotis lucifugus) in urban and non-urban riparian sites in and around Calgary, Alberta, Canada. This species dominated bat assemblages throughout our study area, but nowhere more so than in the city. Our data did not support most of our specific predictions. Increased numbers of urban bats did not reflect urbanization-related benefits such as enhanced body condition, reproductive rates, or successful production of juveniles. Instead, bats did best in the transition zone situated between strictly urban and rural areas. CONCLUSIONS/SIGNIFICANCE: We reject our hypothesis and explore various explanations. One possibility is that urban and rural M. lucifugus exhibit increased use of anthropogenic roosts, as opposed to natural ones, leading to larger maternity colonies and higher population densities and, in turn, increased competition for insect prey. Other possibilities include increased stress, disease transmission and/or impacts of noise on urban bats. Whatever the proximate cause, the combination of greater bat population density with decreased body condition and production of juveniles indicates that Calgary does not represent a population source for Prairie bats. We studied a highly synanthropic species in a system where it could reasonably be expected to respond positively to urbanization, but failed to observe any apparent benefits at the individual level, leading us to propose that urban development may be universally detrimental to bats.

Rabies prevalence in migratory tree-bats in Alberta and the influence of roosting ecology and sampling method on reported prevalence of rabies in bats.

The migratory tree-roosting hoary bat (Lasiurus cinereus) and silver-haired bat (Lasionycteris noctivagans) are among the bat species with the highest reported prevalence of rabies in North America. However, bats submitted for rabies testing typically have been those that have come in contact with humans or pets. Given the roosting ecology of L. cinereus and L. noctivagans, contact with healthy individuals of these species is expected to be rare, with a bias in contact and submission of infected individuals and thus an overestimation of rabies prevalence. We tested 121 L. cinereus and 96 L. noctivagans specimens, collected during mortality surveys at wind energy facilities in Southern Alberta, Canada in 2007 and 2008, for rabies. None of the L. cinereus (0%) and one L. noctivagans (1%) tested positive for rabies. Prevalence of rabies was significantly lower than previously reported estimates, passive and active, for L. cinereus and L. noctivagans. In a review of the literature including multiple bat species, we found a significant difference in estimates of rabies prevalence based on passive versus active surveillance testing. Furthermore, roosting ecology influenced estimates of rabies prevalence, with significantly higher prevalence among passive surveillance submissions of nonsynanthropic species compared to synanthropic species, a trend not evident in active surveillance reports. We conclude that rabies prevalence in randomly collected L. cinereus and L. noctivagans is low and comparable to active surveillance estimates from other species (≤ 1%), and that roosting ecology influences estimates of rabies prevalence among bats submitted to public health laboratories in North America.

The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern?

The peak echolocation frequency of insectivorous bats generally declines as body size increases. However, there are notable exceptions to this rule, with some species, such as Rhinolophus clivosus, having a higher than expected peak frequency for their body size. Such deviations from allometry may be associated with partitioning of foraging habitat (the foraging habitat hypothesis) or insect prey (the prey detection hypothesis). Alternatively, the deviations may be associated with the partitioning of sonar frequency bands to allow effective communication in a social context (the acoustic communication hypothesis). We tested the predictions of these hypotheses through comparisons at the family, clade and species level, using species of rhinolophids in general and R. clivosus, a species with a wide distribution, as a specific test case. We compared the wing parameters, echolocation frequency and ecology of R. clivosus to those of the sympatric R. capensis. Rhinolophus clivosus has a much higher echolocation frequency than predicted from its wing loading or body mass. Furthermore, contrary to the predictions of the foraging habitat hypothesis, we found no difference in foraging habitat between R. clivosus and R. capensis. The size range of insect prey taken by the two species also overlapped almost completely, contrary to the prey detection hypothesis. On the other hand, the variation of echolocation frequencies around the allometric relationship for rhinolophids was smaller than that for Myotis spp., supporting the prediction of the acoustic communication hypothesis. We thus propose that the relatively high peak frequency of R. clivosus is the result of partitioning of sonar frequency bands to minimize the ambiguity of echolocation calls during social interactions.

Genetic analysis reveals demographic fragmentation of grizzly bears yielding vulnerably small populations.

Ecosystem conservation requires the presence of native carnivores, yet in North America, the distributions of many larger carnivores have contracted. Large carnivores live at low densities and require large areas to thrive at the population level. Therefore, if human-dominated landscapes fragment remaining carnivore populations, small and demographically vulnerable populations may result. Grizzly bear range contraction in the conterminous USA has left four fragmented populations, three of which remain along the Canada-USA border. A tenet of grizzly bear conservation is that the viability of these populations requires demographic linkage (i.e. inter-population movement of both sexes) to Canadian bears. Using individual-based genetic analysis, our results suggest this demographic connection has been severed across their entire range in southern Canada by a highway and associated settlements, limiting female and reducing male movement. Two resulting populations are vulnerably small (< or =100 animals) and one of these is completely isolated. Our results suggest that these trans-border bear populations may be more threatened than previously thought and that conservation efforts must expand to include international connectivity management. They also demonstrate the ability of genetic analysis to detect gender-specific demographic population fragmentation in recently disturbed systems, a traditionally intractable yet increasingly important ecological measurement worldwide.