Effects of telemetry collars on two free-roaming feral equid species.

There are two species of free-roaming feral equids in North America: horses (Equus caballus) and donkeys or "burros" (E. asinus). Both species were introduced as domestic animals to North America in the early 1500s and currently inhabit rangelands across the western United States, Canada, and all continents except Antarctica. Despite their global distribution, little is known about their fine scale spatial ecology. Contemporary research tools to assess space use include global positioning system (GPS) tracking collars, but older models were problematic due to stiff collar belting causing poor fit. We tested modern designs of GPS collars on n = 105 horses and n = 60 burros for 4 years in five populations (3 horse, 2 burro) across the western United States, to assess whether collars posed welfare risks to horses or burros. We found no difference in survival of collared versus uncollared mares and jennies, and no difference in survival of their foals. In 4036 of 4307 observations for horses (93.7%) and 2115 of 2258 observations for burros (93.6%), collars were observed symmetrical, maintaining proper fit on the neck. Fur effects from collars (sweaty neck, indented fur, broken fur) were seen in 3% of horse observations and 25% of burro observations. Superficial effects (chafes and marks on skin surface) were seen in 2% of horse observations and 11% of burro observations; no severe effects from collars were seen. Body condition was not affected by collars; mean body condition of collared horses was 4.70 ± 0.54 (mean ± s.d) and 4.71 ± 0.65 for collared burros. Behavior results indicated minimal effects; collared horses stood slightly more than uncollared, and collared burros stood and foraged more in one population, but not in the other. For 6.3% of observations of horses and 6.4% of observations of burros, we found an effect of time wearing a collar on the cumulative sum of fur effects which increased over time (burros: rs = 0.87, P = <0.0001; horses: rs = 0.31, P = 0.002). Burros also showed an increase over time in the number of superficial effects, but horses did not. Collars occasionally moved into the wrong position, shifting forward over the ears; we observed this on 19 horses and 1 burro. Of those, most collars went over the ears in summer (n = 12). All collars were equipped with a remote release mechanism as well as a timed-release mechanism for redundancy, thus removed when observed in wrong position to avoid rubbing or discomfort. Our finding of no consequential physical effects in 98% of horse observations, and 89% of burro observations suggests the consequences of collars on free-roaming equid welfare and survival is biologically insignificant, although collars should be monitored regularly and continue to be equipped with a remote release mechanism to remove a collar if needed. With frequent welfare-driven, visual monitoring, collaring of free-roaming equids can be a safe and useful tool to increase our understanding of their spatial ecology, demography, habitat use, behavior, and interactions with other wildlife.

Drivers of habitat availability for terrestrial mammals: Unravelling the role of livestock, land conversion and intrinsic traits in the past 50 years.

The global decline of terrestrial species is largely due to the degradation, loss and fragmentation of their habitats. The conversion of natural ecosystems for cropland, rangeland, forest products and human infrastructure are the primary causes of habitat deterioration. Due to the paucity of data on the past distribution of species and the scarcity of fine-scale habitat conversion maps, however, accurate assessment of the recent effects of habitat degradation, loss and fragmentation on the range of mammals has been near impossible. We aim to assess the proportions of available habitat within the lost and retained parts of mammals' distribution ranges, and to identify the drivers of habitat availability. We produced distribution maps for 475 terrestrial mammals for the range they occupied 50 years ago and compared them to current range maps. We then calculated the differences in the percentage of 'area of habitat' (habitat available to a species within its range) between the lost and retained range areas. Finally, we ran generalized linear mixed models to identify which variables were more influential in determining habitat availability in the lost and retained parts of the distribution ranges. We found that 59% of species had a lower proportion of available habitat in the lost range compared to the retained range, thus hypothesizing that habitat loss could have contributed to range declines. The most important factors negatively affecting habitat availability were the conversion of land to rangeland and high density of livestock. Significant intrinsic traits were those related to reproductive timing and output, habitat breadth and medium body size. Our findings emphasize the importance of implementing conservation strategies to mitigate the impacts caused by human activities on the habitats of mammals, and offer evidence indicating which species have the potential to reoccupy portions of their former range if other threats cease to occur.

Browsers or Grazers? New Insights into Feral Burro Diet Using a Non-Invasive Sampling and Plant DNA Metabarcoding Approach.

Ungulates play a large role in shaping ecosystems and communities by influencing plant composition, structure, and productivity. We investigated the summer diets of feral burros in two ecosystems in which they are found in the United States: a subtropical desert in Arizona and a temperate juniper shrubland in Utah. Between 24 June and 16 July of 2019, we gathered 50 burro fecal samples from each location and used plant DNA metabarcoding to determine the burros' diets. We found that during our sampling period the burros in the Sonoran Desert consumed a higher proportion of woody browse and had a narrower dietary niche breadth and lower degree of diet diversity compared to the burros in the juniper shrubland ecosystem, where the burros consumed higher proportions of graminoids and forbs and had a higher diet diversity index and broader dietary niche breadth. The burros in the Sonoran Desert relied primarily on Prosopis spp. (mesquite) and Poaceae grasses, whereas the burros in the juniper shrubland relied on a wider variety of forb and grass species, likely due to the greater variability in the forage species temporally and spatially available in that temperate ecosystem. We found that feral burros are highly adaptable with respect to diet and appear to be employing a mixed feeding strategy, similar to their ancestor, the African wild ass, to meet their nutritional needs in whichever ecosystem they are found.

Not just for males: Flehmen as a tool for detection of reproductive status and individual recognition across sexes in four African equid species.

Flehmen is frequently explained as part of male sexual behaviour, but it can also be associated with overmarking behaviour and thus individual recognition. We tested three explanatory hypotheses of flehmen behaviour: to detect sexual status of a female, to decide whether to overmark an individual, and to improve individual recognition. Additionally, we examined interspecific flehmen differences in the African equids. We observed 130 individuals of all 4 species among 15 groups in 5 zoos. We recorded 4445 eliminations: 142 were accompanied by flehmen and 1648 were inspected by another animal and followed by flehmen (n = 147 cases). As males of all age categories flehmened more often than females we conclude that flehmen serves to detect reproductive status of a female. However, this is not an exclusive explanation as animals of all sex and age categories flehmened when inspecting an elimination. Flehmen was not the predictor of overmarking. Nevertheless, we suggest that foals could use it for individual recognition. We found large interspecific differences with the highest rate of flehmen in African wild ass and least in mountain zebra. Thus, while the main function of flehmen is to detect female reproductive status, inter-individual and inter-species differences also play a role.

Why wait to mark? Possible reasons behind latency from olfactory exploration to overmarking in four African equid species.

Whereas most studies on overmarking in mammals analysed the rate of overmarking, that those investigate time between exploration of an olfactory stimulus and the response to it remain less common, with inconsistent results. We examined the latency in time between elimination by the sender and sniffing by the receiver, and from sniffing and overmarking, in four captive African equid species to explore differences among species, and among age and sex classes. We investigated these latency time periods in light of three potential hypotheses explaining overmarking behaviour in equids: social bonds, group cohesion, and intrasexual competition. Analysing 1684 events of sniffing and 719 of overmarking among 130 individuals, we found that (i) the time from elimination to overmarking was shorter among female friends and in parent-offspring dyads, proving support to the social bond hypothesis; (ii) intraspecific differences in time periods do not reflect the social organisation of species, thus not supporting the group cohesion hypothesis; (iii) males were more attracted to elimination of conspecifics than females, and female's eliminations were inspected longer, in line with the sexual competition hypothesis and/or reproductive behaviour. In addition, we found that the younger foals came to sniff eliminations faster than older ones, and in larger groups foals devoted longer time to sniffing the elimination before overmarking. We concluded that examination of the elimination could be driven by motivations other than the decision to overmark. Whereas overmarking serves to express bonds to a familiar individual, the latency of overmarking reflects more reproductive interests.

Body size and digestive system shape resource selection by ungulates: A cross-taxa test of the forage maturation hypothesis.

The forage maturation hypothesis (FMH) states that energy intake for ungulates is maximised when forage biomass is at intermediate levels. Nevertheless, metabolic allometry and different digestive systems suggest that resource selection should vary across ungulate species. By combining GPS relocations with remotely sensed data on forage characteristics and surface water, we quantified the effect of body size and digestive system in determining movements of 30 populations of hindgut fermenters (equids) and ruminants across biomes. Selection for intermediate forage biomass was negatively related to body size, regardless of digestive system. Selection for proximity to surface water was stronger for equids relative to ruminants, regardless of body size. To be more generalisable, we suggest that the FMH explicitly incorporate contingencies in body size and digestive system, with small-bodied ruminants selecting more strongly for potential energy intake, and hindgut fermenters selecting more strongly for surface water.

Unusually large upward shifts in cold-adapted, montane mammals as temperature warms.

The largest and tallest mountain range in the contiguous United States, the Southern Rocky Mountains, has warmed considerably in the past several decades due to anthropogenic climate change. Herein we examine how 47 mammal elevational ranges (27 rodent and 4 shrew species) have changed from their historical distributions (1886-1979) to their contemporary distributions (post 2005) along 2,400-m elevational gradients in the Front Range and San Juan Mountains of Colorado. Historical elevational ranges were based on more than 4,580 georeferenced museum specimen and publication records. Contemporary elevational ranges were based on 7,444 records from systematic sampling efforts and museum specimen records. We constructed Bayesian models to estimate the probability a species was present, but undetected, due to undersampling at each 50-m elevational bin for each time period and mountain range. These models leveraged individual-level detection probabilities, the number and patchiness of detections across 50-m bands of elevation, and a decaying likelihood of presence from last known detections. We compared 95% likelihood elevational ranges between historical and contemporary time periods to detect directional change. Responses were variable as 26 mammal ranges changed upward, 6 did not change, 11 changed downward, and 4 were extirpated locally. The average range shift was 131 m upward, while exclusively montane species shifted upward more often (75%) and displayed larger average range shifts (346 m). The best predictors of upper limit and total directional change were species with higher maximum latitude in their geographic range, montane affiliation, and the study mountain was at the southern edge of their geographic range. Thus, mammals in the Southern Rocky Mountains serve as harbingers of more changes to come, particularly for montane, cold-adapted species in the southern portion of their ranges.

Effect of social organisation on interspecific differences in overmarking behaviour of foals in African equids.

Overmarking remains an unstudied topic in juvenile mammals. We have previously documented a very high rate of overmarking by foals in four captive African equid species: mountain zebra (Equus zebra), plains zebra (Equus quagga), Grévy's zebra (Equus grevyi), and African wild ass (Equus africanus). African equids vary interspecifically in their social organisation. Since differences in social organisation affect many mammalian behaviours, in this study we investigated interspecific differences in overmarking behaviour of foals, analysing only cases where elimination of any other individual was explored by a foal. We hypothesised that the pattern of overmarking by foals should reflect either differences in social organisation of the species or phylogenetic relations among them. We found that in all species very young foals explored mostly maternal eliminations, and this preference declined with increasing age of the foal and reflected the social organisation of the species; the highest overmarking rate was in species with high intragroup aggression (mountain zebra) and lowest in species with low intragroup aggression and which form crèches (African wild ass). Similarly, the rate of overmarking of the mother, as opposed to other herdmates, was associated with social organisation of the respective species. Thus, we found interspecific differences in overmarking by foals, which were associated with variability in social organisation. Since we also revealed differences between African wild ass and zebra behaviour in early stages of ontogeny, we cannot refute the effect of phylogeny on overmarking behaviour. Additionally, our results supported the identity sharing hypothesis as an explanation of overmarking.

Test of four hypotheses to explain the function of overmarking in foals of four equid species.

Overmarking occurs when one individual places its scent mark directly on top of the scent mark of another individual. Although it is almost ubiquitous among terrestrial mammals, we know little about the function of overmarking. In addition, almost all studies on mammalian overmarking behaviour dealt with adult individuals. Reports on this behaviour in juveniles are extremely rare, yet may elucidate the function of this behaviour. We tested four mutually non-exclusive hypotheses which might explain this behaviour in juveniles: (1) conceal the individual's scent identity, (2) announcement of association with other group members, especially the mother-i.e., sharing identity with the mother, (3) to prevent the next conception of the mother, i.e., parent-offspring conflict, and (4) an early expression of male sexual behaviour. We observed 43 foals (out of 108 individuals) from all African equid species (Equus africanus, E. grevyi, E. quagga, E. zebra) in five zoos. In total, we recorded 3340 eliminations; 260 of these events were overmarked by 38 individual foals representing all species. This represents one of the highest rates of overmarking ever recorded by mammalian juveniles. Foals of all species except African wild ass overmarked the mother more often than another herdmate: with male foals overmarked at a higher rate than female foals. Mothers preferred to overmark foals, but not exclusively their own foal. Our results provide support for the hypotheses that overmarking serves to share identity between foal and mother, and that it is an early expression of male sexual behaviour.

Long-term persistence of horse fecal DNA in the environment makes equids particularly good candidates for noninvasive sampling.

Fecal DNA collected noninvasively can provide valuable information about genetic and ecological characteristics. This approach has rarely been used for equids, despite the need for conservation of endangered species and management of abundant feral populations. We examined factors affecting the efficacy of using equid fecal samples for conservation genetics. First, we evaluated two fecal collection methods (paper bag vs. ethanol). Then, we investigated how time since deposition and month of collection impacted microsatellite amplification success and genotyping errors. Between May and November 2014, we collected feral horse fecal samples of known age each month in a feral horse Herd Management Area in western Colorado and documented deterioration in the field with photographs. Samples collected and dried in paper bags had significantly higher amplification rates than those collected and stored in ethanol. There was little difference in the number of loci that amplified per sample between fresh fecal piles and those that had been exposed to the environment for up to 2 months (in samples collected in paper bags). After 2 months of exposure, amplification success declined. When comparing fresh (0-2 months) and old (3-6 months) fecal piles, samples from fresh piles had more matching genotypes across samples, better amplification success and less allelic dropout. Samples defecated during the summer and collected within 2 months of deposition had highest number of genotypes matching among samples, and lowest rates of amplification failure and allelic dropout. Due to the digestive system and amount of fecal material produced by equids, as well as their occurrence in arid ecosystems, we suggest that they are particularly good candidates for noninvasive sampling using fecal DNA.

Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals.

Although habitat fragmentation is often assumed to be a primary driver of extinction, global patterns of fragmentation and its relationship to extinction risk have not been consistently quantified for any major animal taxon. We developed high-resolution habitat fragmentation models and used phylogenetic comparative methods to quantify the effects of habitat fragmentation on the world's terrestrial mammals, including 4,018 species across 26 taxonomic Orders. Results demonstrate that species with more fragmentation are at greater risk of extinction, even after accounting for the effects of key macroecological predictors, such as body size and geographic range size. Species with higher fragmentation had smaller ranges and a lower proportion of high-suitability habitat within their range, and most high-suitability habitat occurred outside of protected areas, further elevating extinction risk. Our models provide a quantitative evaluation of extinction risk assessments for species, allow for identification of emerging threats in species not classified as threatened, and provide maps of global hotspots of fragmentation for the world's terrestrial mammals. Quantification of habitat fragmentation will help guide threat assessment and strategic priorities for global mammal conservation.

Body size and activity times mediate mammalian responses to climate change.

Model predictions of extinction risks from anthropogenic climate change are dire, but still overly simplistic. To reliably predict at-risk species we need to know which species are currently responding, which are not, and what traits are mediating the responses. For mammals, we have yet to identify overarching physiological, behavioral, or biogeographic traits determining species' responses to climate change, but they must exist. To date, 73 mammal species in North America and eight additional species worldwide have been assessed for responses to climate change, including local extirpations, range contractions and shifts, decreased abundance, phenological shifts, morphological or genetic changes. Only 52% of those species have responded as expected, 7% responded opposite to expectations, and the remaining 41% have not responded. Which mammals are and are not responding to climate change is mediated predominantly by body size and activity times (phylogenetic multivariate logistic regressions, P < 0.0001). Large mammals respond more, for example, an elk is 27 times more likely to respond to climate change than a shrew. Obligate diurnal and nocturnal mammals are more than twice as likely to respond as mammals with flexible activity times (P < 0.0001). Among the other traits examined, species with higher latitudinal and elevational ranges were more likely to respond to climate change in some analyses, whereas hibernation, heterothermy, burrowing, nesting, and study location did not influence responses. These results indicate that some mammal species can behaviorally escape climate change whereas others cannot, analogous to paleontology's climate sheltering hypothesis. Including body size and activity flexibility traits into future extinction risk forecasts should substantially improve their predictive utility for conservation and management.