Reciprocated competition between two forest carnivores drives dietary specialization.

Competition shapes animal communities, but the strength of the interaction varies spatially depending on the availability and aggregation of resources and competitors. Among carnivores, competition is particularly pronounced with the strongest interactions between similar species with intermediate differences in body size. While ecologists have emphasized interference competition among carnivores based on dominance hierarchies from body size (smaller = subordinate; larger = dominant), the reciprocity of exploitative competition from subordinate species has been overlooked even though efficient exploitation can limit resource availability and influence foraging. Across North America, fishers Pekania pennanti and martens (Martes spp.) are two phylogenetically related forest carnivores that exhibit a high degree of overlap in habitat use and diet and differ in body size by a factor of 2-5×, eliciting particularly strong interspecific competition. In the Great Lakes region, fishers and martens occur both allopatrically and sympatrically; where they co-occur, the numerically dominant species varies spatially. This natural variation in competitors and environmental conditions enables comparisons to understand how interference and exploitative competition alter dietary niche overlap and foraging strategies. We analysed stable isotopes (δ13 C and δ15 N) from 317 martens and 132 fishers, as well as dietary items (n = 629) from 20 different genera, to compare niche size and overlap. We then quantified individual diet specialization and modelled the response to environmental conditions that were hypothesized to influence individual foraging. Martens and fishers exhibited high overlap in both available and core isotopic δ-space, but no overlap of core dietary proportions. When the competitor was absent or rare, both martens and fishers consumed more smaller-bodied prey. Notably, the dominant fisher switched from being a specialist of larger to smaller prey in the absence of the subordinate marten. Environmental context also influenced dietary specialization: increasing land cover diversity and prey abundance reduced specialization in martens whereas vegetation productivity increased specialization for both martens and fishers. Despite an important dominance hierarchy, fishers adjusted their niche in the face of a subordinate, but superior, exploitative competitor. These findings highlight the underappreciated role of the subordinate competitor in shaping the dietary niche of a dominant competitor.

Seasonality drives the survival landscape of a recovering forest carnivore in a changing world.

Ecological heterogeneity promotes species persistence and diversity. Environmental change has, however, eroded patterns of heterogeneity globally, stifling species recovery. To test the effects of seasonal heterogeneity on a reintroduced carnivore, American martens (Martes americana), we compared metrics of local and season-specific heterogeneity to traditional forest metrics on the survival of 242 individuals across 8 years and predicted a survival landscape for 13 reintroduction sites. We found that heterogeneity-created by forest structure in the growing season and snow in the winter-improved survival and outperformed traditional forest metrics. Spatial variation in heterogeneity created a distinct survival landscape, but seasonal change in heterogeneity generated temporal discordance. All translocation sites possessed high forest heterogeneity but there were greater differences in winter heterogeneity; recovery sites with the poorest snow conditions had the lowest viability. Our work links heterogeneity across seasons to fitness and suggests that management strategies that increase seasonal aspects of heterogeneity may help to recover other sensitive species to continuing environmental change.

A recovery network leads to the natural recolonization of an archipelago and a potential trailing edge refuge.

Rapid environmental change is reshaping ecosystems and driving species loss globally. Carnivore populations have declined and retracted rapidly and have been the target of numerous translocation projects. Success, however, is complicated when these efforts occur in novel ecosystems. Identifying refuges, locations that are resistant to environmental change, within a translocation framework should improve population recovery and persistence. American martens (Martes americana) are the most frequently translocated carnivore in North America. As elsewhere, martens were extirpated across much of the Great Lakes region by the 1930s and, despite multiple translocations beginning in the 1950s, martens remain of regional conservation concern. Surprisingly, martens were rediscovered in 2014 on the Apostle Islands of Lake Superior after a putative absence of >40 yr. To identify the source of martens to the islands and understand connectivity of the reintroduction network, we collected genetic data on martens from the archipelago and from all regional reintroduction sites. In total, we genotyped 483 individual martens, 43 of which inhabited the Apostle Islands (densities 0.42-1.46 km-2 ). Coalescent analyses supported the contemporary recolonization of the Apostle Islands with progenitors likely originating from Michigan, which were sourced from Ontario. We also identified movements by a first-order relative between the Apostle Islands and the recovery network. We detected some regional gene flow, but in an unexpected direction: individuals moving from the islands to the mainland. Our findings suggest that the Apostle Islands were naturally recolonized by progeny of translocated individuals and now act as a source back to the reintroduction sites on the mainland. We suggest that the Apostle Islands, given its protection from disturbance, complex forest structure, and reduced carnivore competition, will act as a potential refuge for marten along their trailing range boundary and a central node for regional recovery. Our work reveals that translocations, even those occurring along southern range boundaries, can create recovery networks that function like natural metapopulations. Identifying refuges, locations that are resistant to environmental change, within these recovery networks can further improve species recovery, even within novel environments. Future translocation planning should a priori identify potential refuges and sources to improve short-term recovery and long-term persistence.

Abiotic conditions mediate intraguild interactions between mammalian carnivores.

Intraguild (IG) interactions are common among mammalian carnivores, can include intraguild predation (IGP) and interspecific killing (IK), and are often asymmetrical, where a larger more dominant species (IGpredator ) kills a smaller one (IGprey ). According to ecological theory, the potential for an IGpredator and IGprey to coexist depends on whether the direct consumptive benefits for the IGpredator are substantial (IGP) or insignificant (IK), the extent to which the IGprey is the superior exploitative competitor on shared prey resources, and overall ecosystem productivity. We used resource selection models and spatially explicit age and harvest data for two closely related mesopredators that engage in IG interactions, American martens (Martes americana; IGprey ) and fishers (Pekania pennanti; IGpredator ), to identify drivers of distributions, delineate areas of sympatry and allopatry, and explore the role of an apex predator (coyote; Canis latrans) on these interactions. Model selection revealed that fisher use of this landscape was strongly influenced by late winter abiotic conditions, but other bottom-up (forest composition) and top-down (coyote abundance) factors also influenced their distribution. Overall, fisher probability of use was higher where late winter temperatures were warmer, snowpack was deeper, and measures of productivity were greater. Martens were constrained to areas of the landscape where the probability of fisher use, coyote abundance, and productivity were low and selected for forest conditions that presumably maximized prey availability. Marten age data indicated an increased proportion of juveniles outside of the predicted area of sympatry, suggesting that few animals survived >1.5 years in this area that supported higher densities of fishers and coyotes. Consistent with asymmetrical IG interaction theory, the IGpredator (fishers and, to a lesser degree, coyotes) competitively excluded the IGprey (martens) from more productive, milder temperature habitats, whereas IGpredators and IGprey coexisted in low productivity environments, where a combination of abiotic and biotic conditions enabled the IGprey to be the superior exploitative competitor.

SEROSURVEY, HEMATOLOGY, AND CAUSES OF MORTALITY OF FREE-RANGING AMERICAN MARTENS ( MARTES AMERICANA) IN MICHIGAN.

To better understand the clinical pathology, diseases, and causes of mortality of reintroduced American martens ( Martes americana) in Michigan, a study was conducted from 2011 to 2015 in the Upper and Lower Peninsulas of Michigan. Samples obtained from live trapping ( n = 58) or harvested carcasses ( n = 34) were serologically tested for select pathogens. Antibodies against Toxoplasma gondii and canine distemper virus were detected in 58 and 3.4% of samples, respectively. All samples were seronegative for Leptospira spp. and negative for Dirofilaria immitis antigen. Urine samples tested for Leptospira spp. via immunofluorescent antibody assay ( n = 7), polymerase chain reaction ( n = 6) , or both ( n = 3) were all negative. Parvovirus DNA was detected in 9.1% of small intestine samples ( n = 22) collected from carcasses and in 3.7% of fecal samples ( n = 27) collected during live trapping. Complete blood counts ( n = 64) and serum biochemistries ( n = 63) were obtained from 49 live-trapped martens. Biochemical parameters found to be significantly different ( P < 0.05) between genders were calcium, creatinine, glucose, and phosphorus. There was no significant difference between genders for any hematologic parameter. Significant differences ( P < 0.05) between summer and winter seasons were found in total estimated white blood cell count, neutrophils, lymphocytes, monocytes, alkaline phosphatase, bicarbonate, calcium, creatinine, globulin, glucose, phosphorus, potassium, sodium, and total protein. There was no significant difference in blood cell count or serum biochemistry values between radio-collared ( n = 17) and noncollared ( n = 47) martens. Animals seropositive for T. gondii were found to have significantly higher ( P < 0.05) eosinophil and globulin levels than seronegative animals. The primary natural cause for mortality of radio-collared American martens was predation. Histologic examinations revealed a high percentage (60%) of martens with verminous or granulomatous pneumonia.

Pairing field methods to improve inference in wildlife surveys while accommodating detection covariance.

It is common to use multiple field sampling methods when implementing wildlife surveys to compare method efficacy or cost efficiency, integrate distinct pieces of information provided by separate methods, or evaluate method-specific biases and misclassification error. Existing models that combine information from multiple field methods or sampling devices permit rigorous comparison of method-specific detection parameters, enable estimation of additional parameters such as false-positive detection probability, and improve occurrence or abundance estimates, but with the assumption that the separate sampling methods produce detections independently of one another. This assumption is tenuous if methods are paired or deployed in close proximity simultaneously, a common practice that reduces the additional effort required to implement multiple methods and reduces the risk that differences between method-specific detection parameters are confounded by other environmental factors. We develop occupancy and spatial capture-recapture models that permit covariance between the detections produced by different methods, use simulation to compare estimator performance of the new models to models assuming independence, and provide an empirical application based on American marten (Martes americana) surveys using paired remote cameras, hair catches, and snow tracking. Simulation results indicate existing models that assume that methods independently detect organisms produce biased parameter estimates and substantially understate estimate uncertainty when this assumption is violated, while our reformulated models are robust to either methodological independence or covariance. Empirical results suggested that remote cameras and snow tracking had comparable probability of detecting present martens, but that snow tracking also produced false-positive marten detections that could potentially substantially bias distribution estimates if not corrected for. Remote cameras detected marten individuals more readily than passive hair catches. Inability to photographically distinguish individual sex did not appear to induce negative bias in camera density estimates; instead, hair catches appeared to produce detection competition between individuals that may have been a source of negative bias. Our model reformulations broaden the range of circumstances in which analyses incorporating multiple sources of information can be robustly used, and our empirical results demonstrate that using multiple field-methods can enhance inferences regarding ecological parameters of interest and improve understanding of how reliably survey methods sample these parameters.

Seasonal shifts in the habitat selection patterns of male American Marten (Martes americana) at a fine spatial scale.

Old-growth forests harbor a large amount of complex structural features that result in a wide array of wildlife habitats. However, intensive forest management is gradually converting old-growth forest into younger, even-aged stands, reducing structural complexity and threatening the persistence of old-growth-dependent species. Maintaining elements of complex stand structure is critical to the conservation of old-growth forest specialists that use different habitat components at different periods of their annual cycle, and it requires a comprehensive understanding of seasonal variation in the habitat needs of these species. However, difficulties in observing free-ranging animals have sometimes limited our ability to assess such variations in habitat requirements, especially for small, elusive species. To address this, we used GPS telemetry collars to describe fine-scale habitat selection patterns of 6 male American Martens (Martes americana) during 2 contrasting periods of the year (snow-free, from mid-April to mid-November; snow-covered, from mid-November to mid-April), an objective formerly hard to achieve using conventional VHF telemetry. We used resource selection functions conducted at the fourth order of selection to compare habitat characteristics found at the sites used by martens (GPS locations, n = 100) to those found on an equal number of available sites (random points, n = 100) within each individual seasonal home range. We conducted vegetation surveys on these 200 sites to describe habitat and built candidate models representing different concurrent hypotheses. Our results showed that proxies of prey availability, predator avoidance, and thermal constraints were the primary factors influencing marten habitat selection during both periods, although their respective importance differed between periods. Martens selected sites with a high density of large-diameter snags (≥30·ha-1), high conifer canopy closure (≥53%), and a dense lateral cover (≥81%) during the snow-free period, but selected sites with a high volume of coarse woody debris (≥64 m3·ha-1) and high conifer canopy closure (≥48%) during the snow-covered period. Our results highlight the importance of contrasting seasonal changes in habitat selection patterns of small carnivores and may help maintain structural attributes in the landscape that are suitable for male American Martens.

BIOACCUMULATION OF MERCURY IN A TERRESTRIAL CARNIVORE, AMERICAN MARTEN (MARTES AMERICANA).

Studies that assess mercury bioaccumulation in small carnivores in terrestrial habitats are limited. We quantified total mercury (THg) in American marten (Martes americana) that were harvested for fur in Michigan, US, during 2013 and 2014. We quantified THg (dry weight) in hair, kidney, and liver samples and further analyzed hair for potential demographic and ecological factors that influence THg bioaccumulation. We found THg concentrations to be the highest in hair (1.228±0.475 µg/g, n=40), followed by kidney (0.922±0.651 µg/g, n=29) and liver (0.344±0.219 µg/g, n=26). Total mercury distributed predictably and significantly between tissue types, and hair was moderately predictive at modeling THg in kidney (R2=0.50, P<0.001, n=29) and weakly predictive in liver (R2=0.35, P<0.001, n=26), suggesting that hair, which is easily obtained, could be a useful sample type for future biomonitoring programs. The concentrations of THg in hair were higher in adults relative to juveniles, and adult female martens had the highest levels of THg (1.980±0.188 µg/g), as compared to juveniles and adult males. Results of generalized linear modeling suggested that THg hair concentrations were positively associated with marten age and trophic position (stable isotope ratio, δ15N). An interaction between δ15N and the year marten carcasses were collected showed that δ15N alone could be highly predictive of THg in some years but not in others. Annual changes in diet could lead to differing rates of mercury bioaccumulation and alter the usefulness of δ15N to predict THg in marten tissues. Further research should explore the connections between changes in prey availability, types of prey consumed, and the influence on bioaccumulation rates of mercury in terrestrial system mesocarnivores.

Carnivore Contact: A Species Fracture Zone Delineated Amongst Genetically Structured North American Marten Populations (Martes americana and Martes caurina).

North American martens are forest dependent, influenced by human activity, and climate vulnerable. They have long been managed and harvested throughout their range as the American marten (Martes americana). Recent work has expanded evidence for the original description of two species in North America - M. americana and the Pacific Coast marten, M. caurina - but the geographic boundary between these groups has not been described in detail. From 2010 to 2016 we deployed 734 multi-taxa winter bait stations across a 53,474 km2 study area spanning seven mountain ranges within the anticipated contact zone along the border of Canada and the United States. We collected marten hair samples and developed genotypes for 15 polymorphic microsatellite loci for 235 individuals, and 493 base-pair sequences of the mtDNA gene COI for 175 of those individuals. Both nuclear and mitochondrial genetic structure identified a sharp break across the Clark Fork Valley, United States with M. americana and M. caurina occurring north and south of the break, respectively. We estimated global effective population size (N e ) for each mountain range, clinal genetic neighborhood sizes (NS), calculated observed (H o ) and expected (H e ) heterozygosity, fixation index (F ST ), and clinal measures of allelic richness (Ar), H o , and inbreeding coefficient (F IS ). Despite substantial genetic structure, we detected hybridization along the fracture zone with both contemporary (nuclear DNA) and historic (mtDNA) gene flow. Marten populations in our study area are highly structured and the break across the fracture zone being the largest documented in North America (F ST range 0.21-0.34, mean = 0.27). With the exception of the Coeur d'Alene Mountains, marten were well distributed across higher elevation portions of our sampling area. Clinal NS values were variable suggesting substantial heterogeneity in marten density and movement. For both M. americana and M. caurina, elevationaly dependent gene flow and high genetic population structure suggest that connectivity corridors will be important to ensuring long-term population persistence. Our study is an example of how a combination of global and clinal molecular data analyses can provide important information for natural resource management.

American marten and fisher do not segregate in space and time during winter in a mixed-forest system.

Understanding the mechanisms of coexistence between ecologically similar species is an important issue in ecology. Carnivore coexistence may be facilitated by spatial segregation, temporal avoidance, and differential habitat selection. American martens Martes americana and fishers Pekania pennanti are medium-sized mustelids that occur sympatrically across portions of North America, yet mechanisms of coexistence between the two species are not fully understood. We assessed spatial and temporal partitioning in martens and fishers in the Upper Peninsula of Michigan, USA, using camera trap data collected during winter 2013-2015. To investigate spatial segregation, we used a dynamic occupancy model to estimate species' occupancy probabilities and probabilities of persistence and colonization as a function of covariates and yearly occupancy probability for the other species. Temporal segregation was assessed by estimating diel activity overlap between species. We found weak evidence of spatial or temporal niche partitioning of martens and fishers. There was high overlap in forest cover selection, and both marten and fisher occupancy were positively correlated with deciduous forests (excluding aspen [Populus tremuloides]). There was strong temporal overlap ( Δ ^ 4 = 0.81 ; CI = 0.79-0.82) with both species exhibiting largely crepuscular activity patterns. Co-occurrence of martens and fishers appears to be facilitated by mechanisms not investigated in this study, such as partitioning of snow features or diet. Our results add additional insights into resource partitioning of mesocarnivores, but further research is required to enhance our understanding of mechanisms that facilitate marten and fisher coexistence.

Temporal plasticity in habitat selection criteria explains patterns of animal dispersal.

Patterns of dispersal behavior are often driven by the composition and configuration of suitable habitat in a matrix of unsuitable habitat. Interactions between animal behavior and landscapes can therefore influence population dynamics, population and species distributions, population genetic structure, and the evolution of behavior. Spatially explicit individual-based models (IBMs) are ideal tools for exploring the effects of landscape structure on dispersal. We developed an empirically parameterized IBM in the modeling framework SEARCH to simulate dispersal of translocated American martens in Wisconsin. We tested the hypothesis that a time-limited disperser should be willing to settle in lower quality habitat over time. To evaluate model performance, we used a pattern-oriented modeling approach. Our best model matched all empirical dispersal patterns (e.g., dispersal distance) except time to settlement. This model incorporated a required search phase as well as the mechanism for declining habitat selectivity over time, which represents the first demonstration of this hypothesis for a vertebrate species. We suggest that temporal plasticity in habitat selectivity allows individuals to maximize fitness by making a tradeoff between habitat quality and risk of mortality. Our IBM is pragmatic in that it addresses a management need for a species of conservation concern. However, our model is also paradigmatic in that we explicitly tested a theory of dispersal behavior. Linking these 2 approaches to ecological modeling can further the utility of individual-based modeling and provide direction for future theoretical and empirical work on animal behavior.

Density and population viability of coastal marten: a rare and geographically isolated small carnivore.

Pacific martens (Martes caurina humboldtensis) in coastal forests of Oregon and northern California in the United States are rare and geographically isolated, prompting a petition for listing under the Endangered Species Act. If listed, regulations have the potential to influence land-use decisions on public and private lands, but no estimates of population size, density, or viability of remnant marten populations are available for evaluating their conservation status. We used GPS and VHF telemetry and spatial mark-resight to estimate home ranges, density, and population size of Pacific martens in the Oregon Dunes National Recreation Area, central coast Oregon, USA. We then estimated population viability at differing levels of human-caused mortality (e.g., vehicle mortality). Marten home ranges were small on average (females = 0.8 km2, males 1.5 km2) and density (1.13 martens/1 km2) was the highest reported for North American populations (M. caurina, M. americana). We estimated 71 adult martens (95% CRI [41-87]) across two subpopulations separated by a large barrier (Umpqua River). Using population viability analysis, extinction risk for a subpopulation of 30 martens, approximately the size of the subpopulation south of the Umpqua River, ranged from 32% to 99% with two or three annual human-caused mortalities within 30 years. Absent population expansion, limiting human-caused mortalities will likely have the greatest conservation impact.

Node-based measures of connectivity in genetic networks.

At-site environmental conditions can have strong influences on genetic connectivity, and in particular on the immigration and settlement phases of dispersal. However, at-site processes are rarely explored in landscape genetic analyses. Networks can facilitate the study of at-site processes, where network nodes are used to model site-level effects. We used simulated genetic networks to compare and contrast the performance of 7 node-based (as opposed to edge-based) genetic connectivity metrics. We simulated increasing node connectivity by varying migration in two ways: we increased the number of migrants moving between a focal node and a set number of recipient nodes, and we increased the number of recipient nodes receiving a set number of migrants. We found that two metrics in particular, the average edge weight and the average inverse edge weight, varied linearly with simulated connectivity. Conversely, node degree was not a good measure of connectivity. We demonstrated the use of average inverse edge weight to describe the influence of at-site habitat characteristics on genetic connectivity of 653 American martens (Martes americana) in Ontario, Canada. We found that highly connected nodes had high habitat quality for marten (deep snow and high proportions of coniferous and mature forest) and were farther from the range edge. We recommend the use of node-based genetic connectivity metrics, in particular, average edge weight or average inverse edge weight, to model the influences of at-site habitat conditions on the immigration and settlement phases of dispersal.

Ketamine and midazolam anesthesia in Pacific martens (Martes caurina).

Abstract The use of midazolam as a tranquilizer for anesthesia in mustelids in conjunction with the cyclohexamine ketamine is not well documented. Because midazolam is fast acting, inexpensive, and quickly metabolized, it may serve as a good alternative to other more commonly used tranquilizers. We trapped and anesthetized 27 Pacific martens (Martes caurina) in Lassen National Forest (northern California, US) August 2010-April 2013. We assessed anesthesia with ketamine at 18 and 25 mg/kg combined with 0.2 mg/kg of midazolam by comparing mean times of induction, return to consciousness, and recovery, plus physiologic parameters. No reversal was used for the midazolam portion of the anesthetic. Mean (±SD) induction for both ketamine dosages was 1.7±0.5 and 1.8±1.0 min, respectively. Return to consciousness mean times were 8.0 min longer (P<0.001) for martens receiving a 25 mg/kg ketamine dosage. Mean recoveries were 15.1 min longer (P<0.003) for the 25 mg/kg ketamine dosage. Physiologic parameter means were similar for both ketamine dosages with no statistically significant differences. Body temperatures and heart and respiratory rates were generally stable, but percentage of oxygen saturation and end tidal carbon dioxide values were below those seen in previous mustelid studies. The combination of ketamine, at both dosages, and midazolam provided reliable field anesthesia for Pacific martens, and supplemental oxygen is recommended as needed.