Decomposition stages as a clue for estimating the post-mortem interval in carcasses and providing accurate bird collision rates.

The estimation of the post-mortem interval is crucial to accurately provide bird collision rates against manmade infrastructures. Standard methodologies recommend initially clearing all carcasses to ensure that subsequent collisions can be attributed to known time intervals. In this study, we propose a more cost-efficient approach aiming to link the decomposition stages as unequivocally as possible to the most likely time elapsed since death. Factors influencing the decomposition stages of bird carcasses were evaluated by means of two experiments. Firstly, we examined carcasses of large birds in three seasons differing in temperature, sun radiation and humidity: summer, autumn and spring. Secondly, we tested the influence of body mass in the same season (spring) using small, medium-sized and large bird carcasses. Results showed that the decomposition score increased monotonically with time, attaining the highest magnitude effect. A carcass with a decomposition score ≥ 4 (skeletal reduction) was in the field for ≥ 15 days, whereas a carcass with a score < 3 (fresh or emphysematous) was exposed < 3 days. Decomposition scores were higher in summer and did not differ among carcass sizes. This study provides an alternative protocol to estimate the post-mortem interval in wild birds in studies in search of bird fatalities.

Significant reductions of host abundance weakly impact infection intensity of Batrachochytrium dendrobatidis.

Infectious diseases are considered major threats to biodiversity, however strategies to mitigate their impacts in the natural world are scarce and largely unsuccessful. Chytridiomycosis is responsible for the decline of hundreds of amphibian species worldwide, but an effective disease management strategy that could be applied across natural habitats is still lacking. In general amphibian larvae can be easily captured, offering opportunities to ascertain the impact of altering the abundance of hosts, considered to be a key parameter affecting the severity of the disease. Here, we report the results of two experiments to investigate how altering host abundance affects infection intensity in amphibian populations of a montane area of Central Spain suffering from lethal amphibian chytridiomycosis. Our laboratory-based experiment supported the conclusion that varying density had a significant effect on infection intensity when salamander larvae were housed at low densities. Our field experiment showed that reducing the abundance of salamander larvae in the field also had a significant, but weak, impact on infection the following year, but only when removals were extreme. While this suggests adjusting host abundance as a mitigation strategy to reduce infection intensity could be useful, our evidence suggests only heavy culling efforts will succeed, which may run contrary to objectives for conservation.

Seasonal migrations, body temperature fluctuations, and infection dynamics in adult amphibians.

Risks of parasitism vary over time, with infection prevalence often fluctuating with seasonal changes in the annual cycle. Identifying the biological mechanisms underlying seasonality in infection can enable better prediction and prevention of future infection peaks. Obtaining longitudinal data on individual infections and traits across seasons throughout the annual cycle is perhaps the most effective means of achieving this aim, yet few studies have obtained such information for wildlife. Here, we tracked spiny common toads (Bufo spinosus) within and across annual cycles to assess seasonal variation in movement, body temperatures and infection from the fungal parasite, Batrachochytrium dendrobatidis (Bd). Across annual cycles, toads did not consistently sustain infections but instead gained and lost infections from year to year. Radio-tracking showed that infected toads lose infections during post-breeding migrations, and no toads contracted infection following migration, which may be one explanation for the inter-annual variability in Bd infections. We also found pronounced seasonal variation in toad body temperatures. Body temperatures approached 0 °C during winter hibernation but remained largely within the thermal tolerance range of Bd. These findings provide direct documentation of migratory recovery (i.e., loss of infection during migration) and escape in a wild population. The body temperature reductions that we observed during hibernation warrant further consideration into the role that this period plays in seasonal Bd dynamics.

Cuckoos host range is associated positively with distribution range and negatively with evolutionary uniqueness.

The evolutionary distinctiveness (ED) score is a measure of phylogenetic isolation that quantifies the evolutionary uniqueness of a species. Here, we compared the ED score of parasitic and non-parasitic cuckoo species world-wide, to understand whether parental care or parasitism represents the largest amount of phylogenetic uniqueness. Next, we focused only on 46 cuckoo species characterized by brood parasitism with a known number of host species, and we explored the associations among ED score, number of host species and breeding range size for these species. We assessed these associations using phylogenetic generalized least squares (PGLS) models, taking into account the phylogenetic signal. Parasitic cuckoo species were not more unique in terms of ED than non-parasitic species. However, we found a significant negative association between the evolutionary uniqueness and host range and a positive correlation between the number of host species and range size of parasitic cuckoos, probably suggesting a passive sampling of hosts by parasitic species as the breeding range broadens. The findings of this study showed that more generalist brood parasites occupied very different positions in a phylogenetic tree, suggesting that they have evolved independently within the Cuculiformes order. Finally, we demonstrated that specialist cuckoo species also represent the most evolutionarily unique species in the order of Cuculiformes.

Habitat suitability-density relationship in an endangered woodland species: the case of the Blue Chaffinch (Fringilla polatzeki).

BACKGROUND: Understanding constraints to the distribution of threatened species may help to ascertain whether there are other suitable sectors for reducing the risks associated with species that are recorded in only one protected locality, and to inform about the suitability of other areas for reintroduction or translocation programs. METHODS: We studied the Gran Canaria blue chaffinch (Fringilla polatzeki), a habitat specialist endemic of the Canary Islands restricted to the pine forest of Inagua, the only area where the species has been naturally present as a regular breeder in the last 25 years. A suitability distribution model using occurrences with demographic relevance (i.e., nest locations of successful breeding attempts analysed using boosted classification trees) was built considering orographic, climatic and habitat structure predictors. By means of a standardized survey program we monitored the yearly abundance of the species in 100 sectors since the declaration of Inagua as a Strict Nature Reserve in 1994. RESULTS: The variables with the highest relative importance in blue chaffinch habitat preferences were pine height, tree cover, altitude, and rainfall during the driest trimester (July-September). The observed local abundance of the blue chaffinch in Inagua (survey data) was significantly correlated with habitat suitability derived from modelling the location of successful nesting attempts (using linear and quantile regressions). The outcomes of the habitat suitability model were used to quantify the suitability of other natural, historic, pine forests of Gran Canaria. Tamadaba is the forest with most suitable woodland patches for the species. We estimated a population size of 195-430 blue chaffinches in Inagua since 2011 (95% CI), the smallest population size of a woodland passerine in the Western Palearctic. DISCUSSION: Habitat suitability obtained from modelling the location of successful breeding attempts is a good surrogate of the observed local abundance during the reproductive season. The outcomes of these models can be used for the identification of potential areas for the reintroduction of the species in other suitable pine forests and to inform forest management practices.

Exoskeleton may influence the internal body temperatures of Neotropical dung beetles (Col. Scarabaeinae).

The insect exoskeleton is a multifunctional coat with a continuum of mechanical and structural properties constituting the barrier between electromagnetic waves and the internal body parts. This paper examines the ability of beetle exoskeleton to regulate internal body temperature considering its thermal permeability or isolation to simulated solar irradiance and infrared radiation. Seven Neotropical species of dung beetles (Coleoptera, Scarabaeinae) differing in colour, surface sculptures, size, sexual dimorphism, period of activity, guild category and altitudinal distribution were studied. Specimens were repeatedly subjected to heating trials under simulated solar irradiance and infrared radiation using a halogen neodymium bulb light with a balanced daylight spectrum and a ceramic infrared heat emitter. The volume of exoskeleton and its weight per volume unit were significantly more important for the heating rate at the beginning of the heating process than for the asymptotic maximum temperature reached at the end of the trials: larger beetles with relatively thicker exoskeletons heated more slowly. The source of radiation greatly influences the asymptotic temperature reached, but has a negligible effect in determining the rate of heat gain by beetles: they reached higher temperatures under artificial sunlight than under infrared radiation. Interspecific differences were negligible in the heating rate but had a large magnitude effect on the asymptotic temperature, only detectable under simulated sun irradiance. The fact that sun irradiance is differentially absorbed dorsally and transformed into heat among species opens the possibility that differences in dorsal exoskeleton would facilitate the heat gain under restrictive environmental temperatures below the preferred ones. The findings provided by this study support the important role played by the exoskeleton in the heating process of beetles, a cuticle able to act passively in the thermal control of body temperature without implying energetic costs and metabolic changes.

Beetle Exoskeleton May Facilitate Body Heat Acting Differentially across the Electromagnetic Spectrum.

Exoskeletons of beetles and their associated morphological characteristics can serve many different functions, including thermoregulation. We study the thermal role of the exoskeleton in 13 Geotrupidae dung beetle species using heating experiments under controlled conditions. The main purpose was to measure the influence of heating sources (solar radiance vs. infrared), animal position (dorsal exposure vs. ventral exposure), species identity, and phylogenetic relationships on internal asymptotic temperatures and heating rates. The thermal response was significantly influenced by phylogenetic relatedness, although it was not affected by the apterous condition. The asymptotic internal temperature of specimens was not affected by the thoracic volume but was significantly higher under simulated sunlight conditions than under infrared radiation and when exposed dorsally as opposed to ventrally. There was thus a significant interaction between heating source and body position. Heating rate was negatively and significantly influenced by thoracic volume, and, although insignificantly slower under simulated sunlight, it was significantly affected by body position, being faster under dorsal exposure. The results constitute the first evidence supporting the hypothesis that the beetle exoskeleton acts differentially across the electromagnetic spectrum determining internal body temperatures. This interesting finding suggests the existence of a kind of passive physiology imposed by the exoskeleton and body size, where interspecific relationships play a minor role.

Preferred temperature and thermal breadth of birds wintering in peninsular Spain: the limited effect of temperature on species distribution.

Background. The availability of environmental energy, as measured by temperature, is expected to limit the abundance and distribution of endotherms wintering at temperate latitudes. A prediction of this hypothesis is that birds should attain their highest abundances in warmer areas. However, there may be a spatial mismatch between species preferred habitats and species preferred temperatures, so some species might end-up wintering in sub-optimal thermal environments. Methods. We model the influence of minimum winter temperature on the relative abundance of 106 terrestrial bird species wintering in peninsular Spain, at 10 ×10 km(2) resolution, using 95%-quantile regressions. We analyze general trends across species on the shape of the response curves, the environmental preferred temperature (at which the species abundance is maximized), the mean temperature in the area of distribution and the thermal breadth (area under the abundance-temperature curve). Results. Temperature explains a low proportion of variation in abundance. The most significant effect is on limiting the maximum potential abundance of species. Considering this upper-limit response, there is a large interspecific variability on the thermal preferences and specialization of species. Overall, there is a preponderance of positive relationships between species abundance and temperature; on average, species attain their maximum abundances in areas 1.9 °C warmer than the average temperature available in peninsular Spain. The mean temperature in the area of distribution is lower than the thermal preferences of the species. Discussion. Many species prefer the warmest areas to overwinter, which suggests that temperature imposes important restrictions to birds wintering in the Iberian Peninsula. However, one third of species overwinter in locations colder than their thermal preferences, probably reflecting the interaction between habitat and thermal requirements. There is a high inter-specific variation in the versatility of species using the available thermal space, and the limited effect of temperature highlights the role of other environmental factors determining species abundance.

A protocol for analysing thermal stress in insects using infrared thermography.

The study of insect responses to thermal stress has involved a variety of protocols and methodologies that hamper the ability to compare results between studies. For that reason, the development of a protocol to standardize thermal assays is necessary. In this sense, infrared thermography solves some of the problems allowing us to take continuous temperature measurements without handling the individuals, an important fact in cold-blooded organisms like insects. Here, we present a working protocol based on infrared thermography to estimate both cold and heat thermal stress in insects. We analyse both the change in the body temperature of individuals and their behavioural response. In addition, we used partial least squares regression for the statistical analysis of our data, a technique that solves the problem of having a large number of variables and few individuals, allowing us to work with rare or endemic species. To test our protocol, we chose two species of congeneric, narrowly distributed dung beetles that are endemic to the southeastern part of the Iberian Peninsula. With our protocol we have obtained five variables in the response to cold and twelve in the response to heat. With this methodology we discriminate between the two flightless species of Jekelius through their thermal response. In response to cold, Jekelius hernandezi showed a higher rate of cooling and reached higher temperatures of stupor and haemolymph freezing than Jekelius punctatolineatus. Both species displayed similar thermoregulation ranges before reaching lethal body temperature with heat stress. Overall, we have demonstrated that infrared thermography is a suitable method to assess insect thermal responses with a high degree of sensitivity, allowing for the discrimination between closely related species.

Low effect of young afforestations on bird communities inhabiting heterogeneous Mediterranean cropland.

Afforestation programs such as the one promoted by the EU Common Agricultural Policy have spread tree plantations on former cropland. These afforestations attract generalist forest and ubiquitous species but may cause severe damage to open habitat species, especially birds of high conservation value. We investigated the effects of young (<20 yr) tree plantations dominated by pine P. halepensis on bird communities inhabiting the adjacent open farmland habitat in central Spain. We hypothesize that pine plantations located at shorter distances from open fields and with larger surface would affect species richness and conservation value of bird communities. Regression models controlling for the influence of land use types around plantations revealed positive effects of higher distance to pine plantation edge on community species richness in winter, and negative effects on an index of conservation concern (SPEC) during the breeding season. However, plantation area did not have any effect on species richness or community conservation value. Our results indicate that the effects of pine afforestation on bird communities inhabiting Mediterranean cropland are diluted by heterogeneous agricultural landscapes.

Short term minimum water temperatures determine levels of infection by the amphibian chytrid fungus in Alytes obstetricans tadpoles.

Amphibians are one of the groups of wildlife most seriously threatened by emerging infectious disease. In particular, chytridiomycosis, caused by the aquatic fungus Batrachochytrium dendrobatidis, is responsible for amphibian species declines on a worldwide scale. Population-level outcomes following the introduction of the pathogen are context dependent and mediated by a large suite of abiotic and biotic variables. In particular, studies have shown that temperature has a key role in determining infection dynamics owing to the ectothermic nature of the amphibian host and temperature-dependency of pathogen growth rates. To assess the temperature-dependent seasonality of infectious burdens in a susceptible host species, we monitored lowland populations of larval midwife toads, Alytes obstetricians, in Central Spain throughout the year. We found that infections were highly seasonal, and inversely correlated against water temperature, with the highest burdens of infection seen during the colder months. Short-term impacts of water-temperature were found, with the minimum temperatures occurring before sampling being more highly predictive of infectious burdens than were longer-term spans of temperature. Our results will be useful for selecting the optimal time for disease surveys and, more broadly, for determining the key periods to undertake disease mitigation.

Occurrence data may provide unreliable thermal preferences and breadth of species.

Accurate information on the thermal preference and specialization of species is needed to understand and predict species geographical range size and vulnerability to climate change. Here we estimate the position and breadth of species within thermal gradients based on the shape of the response curve of species abundance to temperature. The objective of the study is to compare the measurements of this approach based on abundance data with those of the classical approach using species' occurrence data. The relationship between species' relative abundance and minimum winter temperature of 106 bird species wintering in the Iberian Peninsula is modeled at 100 Km2 resolution with quadratic logistic regressions. From these models we calculated the preferred temperature of species as the temperature at which the abundance is maximized, and the thermal breadth of species as the relative area under the temperature-abundance curve. We also estimated the thermal preferences and breadth of species as the average temperature and temperature range of the UTM cells in which the species are present. The abundance-temperature response curves reveal that birds prefer higher temperatures to overwinter, and are more thermally selective, than is measured by the classical approach. Moreover, response curves detect a higher inter-specific variability in both thermal preferences and thermal breadth of species. As occurrence data gives the same weight to cells with one or many individuals, the average temperature of the cells in which the species is present roughly reflects the average temperature in the region of study and not the environmental preferences of species.

Foraging patch selection in winter: a balance between predation risk and thermoregulation benefit.

In winter, foraging activity is intended to optimize food search while minimizing both thermoregulation costs and predation risk. Here we quantify the relative importance of thermoregulation and predation in foraging patch selection of woodland birds wintering in a Mediterranean montane forest. Specifically, we account for thermoregulation benefits related to temperature, and predation risk associated with both illumination of the feeding patch and distance to the nearest refuge provided by vegetation. We measured the amount of time that 38 marked individual birds belonging to five small passerine species spent foraging at artificial feeders. Feeders were located in forest patches that vary in distance to protective cover and exposure to sun radiation; temperature and illumination were registered locally by data loggers. Our results support the influence of both thermoregulation benefits and predation costs on feeding patch choice. The influence of distance to refuge (negative relationship) was nearly three times higher than that of temperature (positive relationship) in determining total foraging time spent at a patch. Light intensity had a negligible and no significant effect. This pattern was generalizable among species and individuals within species, and highlights the preponderance of latent predation risk over thermoregulation benefits on foraging decisions of birds wintering in temperate Mediterranean forests.

Does day length affect winter bird distribution? Testing the role of an elusive variable.

Differences in day length may act as a critical factor in bird biology by introducing time constraints in energy acquisition during winter. Thus, differences in day length might operate as a main determinant of bird abundance along latitudinal gradients. This work examines the influence of day length on the abundance of wintering crested tits (Lophophanes cristatus) in 26 localities of Spanish juniper (Juniperus thurifera) dwarf woodlands (average height of 5 m) located along a latitudinal gradient in the Spanish highlands, while controlling for the influence of food availability, minimum night temperature, habitat structure and landscape characteristics. Top regression models in the AIC framework explained 56% of variance in bird numbers. All models incorporated day length as the variable with the highest magnitude effect. Food availability also played an important role, although only the crop of ripe juniper fruits, but not arthropods, positively affected crested tit abundance. Differences in vegetation structure across localities had also a strong positive effect (average tree height and juniper tree density). Geographical variation in night temperature had no influence on crested tit distribution, despite the low winter temperatures reached in these dwarf forests. This paper demonstrates for the first time that winter bird abundance increases with day length after controlling for the effect of other environmental variables. Winter average difference in day length was only 10.5 minutes per day along the 1°47' latitudinal interval (190 km) included in this study. This amount of time, which reaches 13.5 h accumulated throughout the winter season, appears to be large enough to affect the long-term energy budget of small passerines during winter and to shape the distribution of winter bird abundance under restrictive environmental conditions.

The effects of latitude and day length on fattening strategies of wintering coal tits Periparus ater (L.): a field study and aviary experiment.

1. Cyclic daily fattening routines are very common in wintering small wild birds, and are thought to be the consequence of a trade-off between different environmental and state-dependent factors. According to theory, these trajectories should range from accelerated (i.e. mass increases exponentially towards dusk) when mass-dependent predation costs are the most important cause of mortality risk, to decelerated (i.e. the rate of mass gain is highest at dawn and decreases afterward) when starvation is the greater risk. 2. We examine if geographically separate populations of coal tits, wintering in Scotland and central Spain under contrasting photoperiods, show differences in their strategies of daily mass regulation. We describe population differences in wild birds under natural conditions, and experimentally search for interpopulation variation in diurnal body mass increase under common, manipulated, photoperiod conditions (LD 9 : 15 h vs. 7 : 17 h), controlling for temperature, food availability, predator pressure and foraging arena. 3. Winter diurnal mass gain of wild coal tits was more delayed towards the latter part of the daylight period in central Spain (i.e. the locality with longer winter days) than in Scotland. In both localities, the pattern was linked to the average mass at dawn, with mass increasing more rapidly in lighter birds. However, under the controlled photoperiod situation the pattern of daily mass gain was similar in both populations. Diurnal body mass gain was more accelerated at the end of the day, and the increase in body mass in the first hour of the day was considerably lower under the long (9 h) than under the short (7 h) photoperiod in both populations. 4. Wintering coal tits show patterns of mass gain through the day that are compatible with current theories of the costs and benefits of fat storage, with birds at lower latitudes (with longer winter days) having a greater tendency to delay mass gain until late in the day. The experimental study revealed that these patterns are plastic, with birds responding directly to the photoperiod that they experience, suggesting that they are continually making fine-scale adjustments to energy reserves on the basis of both inherent (e.g. state-dependent) and extrinsic cues.

Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link?

Amphibian species are declining at an alarming rate on a global scale in large part owing to an infectious disease caused by the chytridiomycete fungus, Batrachochytrium dendrobatidis. This disease of amphibians has recently emerged within Europe, but knowledge of its effects on amphibian assemblages remains poor. Importantly, little is known about the environmental envelope that is associated with chytridiomycosis in Europe and the potential for climate change to drive future disease dynamics. Here, we use long-term observations on amphibian population dynamics in the Peñalara Natural Park, Spain, to investigate the link between climate change and chytridiomycosis. Our analysis shows a significant association between change in local climatic variables and the occurrence of chytridiomycosis within this region. Specifically, we show that rising temperature is linked to the occurrence of chytrid-related disease, consistent with the chytrid-thermal-optimum hypothesis. We show that these local variables are driven by general circulation patterns, principally the North Atlantic Oscillation. Given that B. dendrobatidis is known to be broadly distributed across Europe, there is now an urgent need to assess the generality of our finding and determine whether climate-driven epidemics may be expected to impact on amphibian species across the wider region.

Influence of heat transmission mode on heating rates and on the selection of patches for heating in a mediterranean lizard.

Heliothermy (heat gain by radiation) has been given a prominent role in basking lizards. However, thigmothermy (heat gain by conduction) could be relevant for heating in small lizards. To ascertain the importance of the different heat transmission modes to the thermoregulatory processes, we conducted an experimental study where we analyzed the role of heat transmission modes on heating rates and on the selection of sites for heating in the Mediterranean lizard Acanthodactylus erythrurus (Lacertidae). The study was conducted under laboratory conditions, where two situations of different operative temperatures (38 degrees and 50 degrees C) were simulated in a terrarium. In a first experiment, individuals were allowed to heat up during 2 min at both temperatures and under both heat transmission modes. In a second experiment, individuals were allowed to select between patches differing in the main transmission mode, at both temperatures, to heat up. Experiences were conducted with live, nontethered lizards with a starting body temperature of 27 degrees C. Temperature had a significant effect on the heating rate, with heat gain per unit of time being faster at the higher operative temperature (50 degrees C). The effect of the mode of heat transmission on the heating rate was also significant: at 50 degrees C, heating rate was greater when the main heat transmission mode was conduction from the substrate (thigmothermy) than when heating was mainly due to heat gain by radiation (heliothermy); at 38 degrees C, heating rates did not significantly differ between transmission modes. At 38 degrees C, selection of the site for heating was not significantly different from that expected by chance. However, at 50 degrees C, the heating site offering the slowest heating rate (heliothermic patch) was selected. These results show that heating rates vary not only with environmental temperature but also with different predominant heat transmission modes. Lizards are able to identify and exploit this heterogeneity, selecting the source of heat gain (radiation) that minimizes the risk of overheating when temperature is high.

Variation in the effect of profitability on prey size selection by the lacertid lizard Psammodromus algirus.

Maximizing the average rate of energy intake (profitability) may not always be the optimal foraging strategy for ectotherms with relatively low energy requirements. To test this hypothesis, we studied the feeding behaviour of captive insectivorous lizards Psammodromus algirus, and we obtained experimental estimates of prey mass, handling time, profitability, and attack distance for several types of prey. Handling time increased linearly with prey mass and differed significantly among prey types when prey size differences were controlled for, and mean profitabilities differed among prey taxa, but profitability was independent of prey size. The attack distance increased with prey length and with the mobility of prey, but it was unrelated to profitability. Thus, lizards did not seem to take account of the rate of energy intake per second as a proximate cue eliciting predatory behavior. This information was combined with pitfall-trap censuses of prey (in late April, mid-June and late July) that allowed us to compare the mass of the prey captured in the environment with that of the arthropods found in the stomachs of sacrificed free-living lizards. In April, when food abundance was low and lizards were reproducing, profitability had a pronounced effect on size selection and lizards selected prey larger than average from all taxa except the least profitable ones. As the active season progressed, and with a higher availability of food, the number of prey per stomach decreased and their mean ize increased. The effect of profitability on size selection decreased (June) and eventually vanished (July-August). This variation is probably related to seasonal changes in the ecology of lizards, e.g. time minimization in the breeding season as a means of saving time for nonforaging activities versus movement minimization by selecting fewer (but larger) prey in the postbreeding season. Thus, the hypothesis that maximizing profitability could be just an optional strategy for a terrestrial ectothermic vertebrate was supported by our data.