A seasonal pulse of ungulate neonates influences space use by carnivores in a multi-predator, multi-prey system.

The behavioral mechanisms by which predators encounter prey are poorly resolved. In particular, the extent to which predators engage in active search for prey versus incidentally encountering them has not been well studied in many systems and particularly not for neonate prey during the birth pulse. Parturition of many large herbivores occurs during a short and predictable temporal window in which young are highly vulnerable to predation. Our study aims to determine how a suite of carnivores responds to the seasonal pulse of newborn ungulates using contemporaneous global positioning system (GPS) locations of four species of predators and two species of prey. We used step-selection functions to assess whether coyotes, cougars, black bears, and bobcats encountered parturient adult female ungulates more often than expected by chance in a low-density population of mule deer and a high-density population of elk. We then assessed whether the carnivore species that encountered parturient prey more often than expected by chance did so by shifting their habitat use toward areas with a high probability of encountering neonates. None of the four carnivore species encountered GPS-collared parturient mule deer more often than expected by chance. By contrast, we determined that cougar and male bear movements positioned them in the proximity of GPS-collared parturient elk more often than expected by chance which may provide evidence of searching behavior. Although both male bears and cougars exhibited behavior consistent with active search for neonates, only male bears used elk parturition habitat in a way that dynamically tracked the phenology of the elk birth pulse suggesting that maximizing encounters with juvenile elk was a motivation when selecting resources. Our results suggest that there is high interspecific and intersexual variability in foraging strategies among large mammalian predators and their prey.

Standardizing protocols for determining the cause of mortality in wildlife studies.

Mortality site investigations of telemetered wildlife are important for cause-specific survival analyses and understanding underlying causes of observed population dynamics. Yet, eroding ecoliteracy and a lack of quality control in data collection can lead researchers to make incorrect conclusions, which may negatively impact management decisions for wildlife populations. We reviewed a random sample of 50 peer-reviewed studies published between 2000 and 2019 on survival and cause-specific mortality of ungulates monitored with telemetry devices. This concise review revealed extensive variation in reporting of field procedures, with many studies omitting critical information for the cause of mortality inference. Field protocols used to investigate mortality sites and ascertain the cause of mortality are often minimally described and frequently fail to address how investigators dealt with uncertainty. We outline a step-by-step procedure for mortality site investigations of telemetered ungulates, including evidence that should be documented in the field. Specifically, we highlight data that can be useful to differentiate predation from scavenging and more conclusively identify the predator species that killed the ungulate. We also outline how uncertainty in identifying the cause of mortality could be acknowledged and reported. We demonstrate the importance of rigorous protocols and prompt site investigations using data from our 5-year study on survival and cause-specific mortality of telemetered mule deer (Odocoileus hemionus) in northern California. Over the course of our study, we visited mortality sites of neonates (n = 91) and adults (n = 23) to ascertain the cause of mortality. Rapid site visitations significantly improved the successful identification of the cause of mortality and confidence levels for neonates. We discuss the need for rigorous and standardized protocols that include measures of confidence for mortality site investigations. We invite reviewers and journal editors to encourage authors to provide supportive information associated with the identification of causes of mortality, including uncertainty.

Variable strategies to solve risk-reward tradeoffs in carnivore communities.

Mesopredator release theory suggests that dominant predators suppress subordinate carnivores and ultimately shape community dynamics, but the assumption that subordinate species are only negatively affected ignores the possibility of facilitation through scavenging. We examined the interplay within a carnivore community consisting of cougars, coyotes, black bears, and bobcats using contemporaneous Global Positioning System telemetry data from 51 individuals; diet analysis from 972 DNA-metabarcoded scats; and data from 128 physical investigations of cougar kill sites, 28 of which were monitored with remote cameras. Resource provisioning from competitively dominant cougars to coyotes through scavenging was so prolific as to be an overwhelming determinant of coyote behavior, space use, and resource acquisition. This was evident via the strong attraction of coyotes to cougar kill sites, frequent scavenging of cougar-killed prey, and coyote diets that nearly matched cougars in the magnitude of ungulate consumption. Yet coyotes were often killed by cougars and used space to minimize encounters, complicating the fitness benefits gained from scavenging. We estimated that 23% (95% CI: 8 to 55%) of the coyote population in our study area was killed by cougars annually, suggesting that coyote interactions with cougars are a complex behavioral game of risk and reward. In contrast, we found no indication that bobcat space use or diet was influenced by cougars. Black bears avoided cougars, but there was no evidence of attraction to cougar kill sites and much lower levels of ungulate consumption and carcass visitation than for coyotes. Interspecific interactions among carnivores are multifaceted, encompassing both suppression and facilitation.

Evaluating and integrating spatial capture-recapture models with data of variable individual identifiability.

Spatial capture-recapture (SCR) models have become the preferred tool for estimating densities of carnivores. Within this family of models are variants requiring identification of all individuals in each encounter (SCR), a subset of individuals only (generalized spatial mark-resight, gSMR), or no individual identification (spatial count or spatial presence-absence). Although each technique has been shown through simulation to yield unbiased results, the consistency and relative precision of estimates across methods in real-world settings are seldom considered. We tested a suite of models ranging from those only requiring detections of unmarked individuals to others that integrate remote camera, physical capture, genetic, and global positioning system (GPS) data into a hybrid model, to estimate population densities of black bears, bobcats, cougars, and coyotes. For each species, we genotyped fecal DNA collected with detection dogs during a 20-d period. A subset of individuals from each species was affixed with GPS collars bearing unique markings and resighted by remote cameras over 140 d contemporaneous with scat collection. Camera-based gSMR models produced density estimates that differed by <10% from genetic SCR for bears, cougars, and coyotes once important sources of variation (sex or behavioral status) were controlled for. For bobcats, SCR estimates were 33% higher than gSMR. The cause of the discrepancies in estimates was likely attributable to challenges designing a study compatible for species with disparate home range sizes and the difficulty of collecting sufficient data in a timeframe in which demographic closure could be assumed. Unmarked models estimated densities that varied greatly from SCR, but estimates became more consistent in models wherein more individuals were identifiable. Hybrid models containing all data sources exhibited the most precise estimates for all species. For studies in which only sparse data can be obtained and the strictest model assumptions are unlikely to be met, we suggest researchers use caution making inference from models lacking individual identity. For best results, we further recommend the use of methods requiring at least a subset of the population is marked and that multiple data sets are incorporated when possible.

Camera trap placement and the potential for bias due to trails and other features.

Camera trapping has become an increasingly widespread tool for wildlife ecologists, with large numbers of studies relying on photo capture rates or presence/absence information. It is increasingly clear that camera placement can directly impact this kind of data, yet these biases are poorly understood. We used a paired camera design to investigate the effect of small-scale habitat features on species richness estimates, and capture rate and detection probability of several mammal species in the Shenandoah Valley of Virginia, USA. Cameras were deployed at either log features or on game trails with a paired camera at a nearby random location. Overall capture rates were significantly higher at trail and log cameras compared to their paired random cameras, and some species showed capture rates as much as 9.7 times greater at feature-based cameras. We recorded more species at both log (17) and trail features (15) than at their paired control cameras (13 and 12 species, respectively), yet richness estimates were indistinguishable after 659 and 385 camera nights of survey effort, respectively. We detected significant increases (ranging from 11-33%) in detection probability for five species resulting from the presence of game trails. For six species detection probability was also influenced by the presence of a log feature. This bias was most pronounced for the three rodents investigated, where in all cases detection probability was substantially higher (24.9-38.2%) at log cameras. Our results indicate that small-scale factors, including the presence of game trails and other features, can have significant impacts on species detection when camera traps are employed. Significant biases may result if the presence and quality of these features are not documented and either incorporated into analytical procedures, or controlled for in study design.

A two-species occupancy model accommodating simultaneous spatial and interspecific dependence.

Occupancy models are popular for estimating the probability a site is occupied by a species of interest when detection is imperfect. Occupancy models have been extended to account for interacting species and spatial dependence but cannot presently allow both factors to act simultaneously. We propose a two-species occupancy model that accommodates both interspecific and spatial dependence. We use a point-referenced multivariate hierarchical spatial model to account for both spatial and interspecific dependence. We model spatial random effects with predictive process models and use probit regression to improve efficiency of posterior sampling. We model occupancy probabilities of red fox (Vulpes vulpes) and coyote (Canis latrans) with camera trap data collected from six mid-Atlantic states in the eastern United States. We fit four models comprising a fully factorial combination of spatial and interspecific dependence to two-thirds of camera trapping sites and validated models with the remaining data. Red fox and coyotes each exhibited spatial dependence at distances > 0.8 and 0.4 km, respectively, and exhibited geographic variation in interspecific dependence. Consequently, predictions from the model assuming simultaneous spatial and interspecific dependence best matched test data observations. This application highlights the utility of simultaneously accounting for spatial and interspecific dependence.

Hidden in plain sight: Cryptic and endemic malaria parasites in North American white-tailed deer (Odocoileus virginianus).

Malaria parasites of the genus Plasmodium are diverse in mammal hosts, infecting five mammalian orders in the Old World, but were long considered absent from the diverse deer family (Cervidae) and from New World mammals. There was a description of a Plasmodium parasite infecting a single splenectomized white-tailed deer (WTD; Odocoileus virginianus) in 1967 but none have been reported since, which has proven a challenge to our understanding of malaria parasite biogeography. Using both microscopy and polymerase chain reaction, we screened a large sample of native and captive ungulate species from across the United States for malaria parasites. We found a surprisingly high prevalence (up to 25%) and extremely low parasitemia of Plasmodium parasites in WTD throughout the eastern United States. We did not detect infections in the other ungulate species nor in western WTD. We also isolated the parasites from the mosquito Anopheles punctipennis. Morphologically, the parasites resemble the parasite described in 1967, Plasmodium odocoilei. Our analysis of the cytochrome b gene revealed two divergent Plasmodium clades in WTD representative of species that likely diverged 2.3 to 6 million years ago, concurrent with the arrival of the WTD ancestor into North America across Beringia. Multigene phylogenetic analysis placed these clades within the larger malaria parasite clade. We document Plasmodium parasites to be common in WTD, endemic to the New World, and as the only known malaria parasites from deer (Cervidae). These findings reshape our knowledge of the phylogeography of the malaria parasites and suggest that other mammal taxa may harbor infection by endemic and occult malaria parasites.