Human disturbance has contrasting effects on niche partitioning within carnivore communities.

Among species, coexistence is driven partly by the partitioning of available resources. The mechanisms of coexistence and competition among species have been a central topic within community ecology, with particular focus on mammalian carnivore community research. However, despite growing concern regarding the impact of humans on the behaviour of species, very little is known about the effect of humans on species interactions. The aim of this review is to establish a comprehensive framework for the impacts of human disturbance on three dimensions (spatial, temporal and trophic) of niche partitioning within carnivore communities and subsequent effects on both intraguild competition and community structure. We conducted a systematic review of the literature on carnivore niche partitioning (246 studies) and extracted 46 reported effects of human disturbance. We found evidence that human disturbance impacts resource partitioning, either positively or negatively, in all three niche dimensions. The repercussions of such variations are highly heterogeneous and differ according to both the type of human disturbance and how the landscape and/or availability of resources are affected. We propose a theoretical framework of the three main outcomes for the impacts of human disturbance on intraguild competition and carnivore community structure: (i) human disturbance impedes niche partitioning, increasing intraguild competition and reducing the richness and diversity of the community; (ii) human disturbance unbalances niche partitioning and intraguild competition, affecting community stability; and (iii) human disturbance facilitates niche partitioning, decreasing intraguild competition and enriching the community. We call for better integration of the impact of humans on carnivore communities in future research on interspecific competition.

Alternated selection mechanisms maintain adaptive diversity in different demographic scenarios of a large carnivore.

BACKGROUND: Different population trajectories are expected to impact the signature of neutral and adaptive processes at multiple levels, challenging the assessment of the relative roles of different microevolutionary forces. Here, we integrate adaptive and neutral variability patterns to disentangle how adaptive diversity is driven under different demographic scenarios within the Iberian wolf (Canis lupus) range. We studied the persistent, the expanding and a small, isolated group within the Iberian wolf population, using 3 MHC class II genes (DRB1, DQA1, and DQB1), which diversity was compared with 39 microsatellite loci. RESULTS: Both the persistent and the expanding groups show evidence of balancing selection, revealed by a significant departure from neutrality at MHC loci, significant higher observed and expected heterozygosity and lower differentiation at MHC than at neutral loci, and signs of positive selection. However, despite exhibiting a significantly higher genetic diversity than the isolated group, the persistent group did not show significant excess of MHC heterozygotes. The expanding group, while showing a similar level of genetic diversity than the persistent group, displays by contrast a significant excess of MHC heterozygotes, which is compatible with the heterozygote advantage mechanism. Results are not clear regarding the role of drift and selection in the isolated group due to the small size of this population. Although diversity indices of MHC loci correspond to neutral expectations in the isolated group, accelerated MHC divergence, revealed by a higher differentiation at MHC than neutral loci, may indicate diversifying selection. CONCLUSION: Different selective pressures were observed in the three different demographic scenarios, which are possibly driven by different selection mechanisms to maintain adaptive diversity.

Gray wolf mortality patterns in Wisconsin from 1979 to 2012.

Starting in the 1970s, many populations of large-bodied mammalian carnivores began to recover from centuries of human-caused eradication and habitat destruction. The recovery of several such populations has since slowed or reversed due to mortality caused by humans. Illegal killing (poaching) is a primary cause of death in many carnivore populations. Law enforcement agencies face difficulties in preventing poaching and scientists face challenges in measuring it. Both challenges are exacerbated when evidence is concealed or ignored. We present data on deaths of 937 Wisconsin gray wolves (Canis lupus) from October 1979 to April 2012 during a period in which wolves were recolonizing historic range mainly under federal government protection. We found and partially remedied sampling and measurement biases in the source data by reexamining necropsy reports and reconstructing the numbers and causes of some wolf deaths that were never reported. From 431 deaths and disappearances of radiocollared wolves aged > 7.5 months, we estimated human causes accounted for two-thirds of reported and reconstructed deaths, including poaching in 39-45%, vehicle collisions in 13%, legal killing by state agents in 6%, and nonhuman causes in 36-42%. Our estimate of poaching remained an underestimate because of persistent sources of uncertainty and systematic underreporting. Unreported deaths accounted for over two-thirds of all mortality annually among wolves > 7.5 months old. One-half of all poached wolves went unreported, or > 80% of poached wolves not being monitored by radiotelemetry went unreported. The annual mortality rate averaged 18% ± 10% for monitored wolves but 47% ± 19% for unmonitored wolves. That difference appeared to be due largely to radiocollaring being concentrated in the core areas of wolf range, as well as higher rates of human-caused mortality in the periphery of wolf range. We detected an average 4% decline in wolf population growth in the last 5 years of the study. Because our estimates of poaching risk and overall mortality rate exceeded official estimates after 2012, we present all data for transparency and replication. More recent additions of public hunting quotas after 2012 appear unsustainable without effective curtailment of poaching. Effective antipoaching enforcement will require more accurate estimates of poaching rate, location, and timing than currently available. Independent scientific review of methods and data will improve antipoaching policies for large carnivore conservation, especially for controversial species facing high levels of human-induced mortality.

Predators and the public trust.

Many democratic governments recognize a duty to conserve environmental resources, including wild animals, as a public trust for current and future citizens. These public trust principles have informed two centuries of U.S.A. Supreme Court decisions and environmental laws worldwide. Nevertheless numerous populations of large-bodied, mammalian carnivores (predators) were eradicated in the 20th century. Environmental movements and strict legal protections have fostered predator recoveries across the U.S.A. and Europe since the 1970s. Now subnational jurisdictions are regaining management authority from central governments for their predator subpopulations. Will the history of local eradication repeat or will these jurisdictions adopt public trust thinking and their obligation to broad public interests over narrower ones? We review the role of public trust principles in the restoration and preservation of controversial species. In so doing we argue for the essential roles of scientists from many disciplines concerned with biological diversity and its conservation. We look beyond species endangerment to future generations' interests in sustainability, particularly non-consumptive uses. Although our conclusions apply to all wild organisms, we focus on predators because of the particular challenges they pose for government trustees, trust managers, and society. Gray wolves Canis lupus L. deserve particular attention, because detailed information and abundant policy debates across regions have exposed four important challenges for preserving predators in the face of interest group hostility. One challenge is uncertainty and varied interpretations about public trustees' responsibilities for wildlife, which have created a mosaic of policies across jurisdictions. We explore how such mosaics have merits and drawbacks for biodiversity. The other three challenges to conserving wildlife as public trust assets are illuminated by the biology of predators and the interacting behavioural ecologies of humans and predators. The scientific community has not reached consensus on sustainable levels of human-caused mortality for many predator populations. This challenge includes both genuine conceptual uncertainty and exploitation of scientific debate for political gain. Second, human intolerance for predators exposes value conflicts about preferences for some wildlife over others and balancing majority rule with the protection of minorities in a democracy. We examine how differences between traditional assumptions and scientific studies of interactions between people and predators impede evidence-based policy. Even if the prior challenges can be overcome, well-reasoned policy on wild animals faces a greater challenge than other environmental assets because animals and humans change behaviour in response to each other in the short term. These coupled, dynamic responses exacerbate clashes between uses that deplete wildlife and uses that enhance or preserve wildlife. Viewed in this way, environmental assets demand sophisticated, careful accounting by disinterested trustees who can both understand the multidisciplinary scientific measurements of relative costs and benefits among competing uses, and justly balance the needs of all beneficiaries including future generations. Without public trust principles, future trustees will seldom prevail against narrow, powerful, and undemocratic interests. Without conservation informed by public trust thinking predator populations will face repeated cycles of eradication and recovery. Our conclusions have implications for the many subfields of the biological sciences that address environmental trust assets from the atmosphere to aquifers.

Intensity of space use reveals conditional sex-specific effects of prey and conspecific density on home range size.

Home range (HR) size variation is often linked to resource abundance, with sex differences expected to relate to sex-specific fitness consequences. However, studies generally fail to disentangle the effects of the two main drivers of HR size variation, food and conspecific density, and rarely consider how their relative influence change over spatiotemporal scales. We used location data from 77 Eurasian lynx (Lynx lynx) from a 16-year Scandinavian study to examine HR sizes variation relative to prey and conspecific density at different spatiotemporal scales. By varying the isopleth parameter (intensity of use) defining the HR, we show that sex-specific effects were conditional on the spatial scale considered. Males had larger HRs than females in all seasons. Females' total HR size declined as prey and conspecific density increased, whereas males' total HR was only affected by conspecific density. However, as the intensity of use within the HR increased (from 90% to 50% isopleth), the relationship between prey density and area showed opposing patterns for females and males; for females, the prey density effect was reduced, while for males, prey became increasingly important. Thus, prey influenced the size of key regions within male HRs, despite total HR size being independent of prey density. Males reduced their HR size during the mating season, likely to remain close to individual females in estrous. Females reduced their HR size postreproduction probably because of movement constrains imposed by dependent young. Our findings highlight the importance of simultaneously considering resources and intraspecific interactions as HR size determinants. We show that sex-specific demands influence the importance of prey and conspecific density on space use at different spatiotemporal scales. Thus, unless a gradient of space use intensity is examined, factors not related to total HR size might be disregarded despite their importance in determining size of key regions within the HR.

A New Method for Noninvasive Genetic Sampling of Saliva in Ecological Research.

Noninvasive samples for genetic analyses have become essential to address ecological questions. Popular noninvasive samples such as faeces contain degraded DNA which may compromise genotyping success. Saliva is an excellent alternative DNA source but scarcity of suitable collection methods makes its use anecdotal in field ecological studies. We develop a noninvasive method of collection that combines baits and porous materials able to capture saliva. We report its potential in optimal conditions, using confined dogs and collecting saliva early after deposition. DNA concentration in saliva extracts was generally high (mean 14 ng µl(-1)). We correctly identified individuals in 78% of samples conservatively using ten microsatellite loci, and 90% of samples using only eight loci. Consensus genotypes closely matched reference genotypes obtained from hair DNA (99% of identification successes and 91% of failures). Mean genotyping effort needed for identification using ten loci was 2.2 replicates. Genotyping errors occurred at a very low frequency (allelic dropout: 2.3%; false alleles: 1.5%). Individual identification success increased with duration of substrate handling inside dog's mouth and the volume of saliva collected. Low identification success was associated with baits rich in DNA-oxidant polyphenols and DNA concentrations <1 ng µl(-1). The procedure performed at least as well as other noninvasive methods, and could advantageously allow detection of socially low-ranked individuals underrepresented in sources of DNA that are involved in marking behaviour (faeces or urine). Once adapted and refined, there is promise for this technique to allow potentially high rates of individual identification in ecological field studies requiring noninvasive sampling of wild vertebrates.

Revisiting food-based models of territoriality in solitary predators.

Food availability is considered a major factor determining spacing behaviour in territorial species, especially for females. Theoretically, spatial overlap (considered the opposite of territoriality) and food availability are related in a nonlinear manner (hypothesized inverted-U function), with high overlap levels at the extremes of a food availability gradient and low overlap at intermediate levels of this gradient. Similar patterns are expected for encounter frequencies owing to its expected correlation with spatial overlap. However, these predictions have rarely been tested in highly structured social systems on a broad gradient of food availability, which implicitly requires experimental manipulation. We test these predictions in a solitary, territorial and trophic specialist, the Iberian lynx Lynx pardinus, taking advantage of a three-decade data set of spatial behaviour in different scenarios of food availability (i.e. rabbit density). In contrast with expectations, home range overlap among resident females was low (median overlap index = 0.08, range 0-0.57) and core area overlap was nearly nil (median overlap index = 0, range 0-0.22) throughout the entire gradient of prey availability. Furthermore, spatial associations between pairs of females were negligible regardless marked variation in prey availability. Therefore, we did not find support for a model of flexible lynx territoriality driven by food availability. Our results suggest that the exclusive use of space in the Iberian lynx was not related to food. Lack of influence of prey availability on lynx territoriality may be adaptive to cope with the consequences of frequent drought-induced periods of prey scarcity or other disturbance typically affecting wild rabbit populations in Mediterranean environments. Thus, lynx would adopt an obstinate strategy of territoriality that consists in defending exclusive areas across a broad range of resource availability ensuring an exclusive access to the minimum amount of prey necessary for survival and eventually reproduction even during periods of prey scarcity. However, we found signs that territoriality was influenced by lynx density in a nonlinear fashion. Our results suggest the occurrence of population regulation through territoriality in this species.

Functional diversity among seed dispersal kernels generated by carnivorous mammals.

1. Knowledge of the spatial scale of the dispersal service provided by important seed dispersers (i.e. common and/or keystone species) is essential to our understanding of their role on plant ecology, ecosystem functioning and, ultimately, biodiversity conservation. 2. Carnivores are the main mammalian frugivores and seed dispersers in temperate climate regions. However, information on the seed dispersal distances they generate is still very limited. We focused on two common temperate carnivores differing in body size and spatial ecology - red fox (Vulpes vulpes) and European pine marten (Martes martes) - for evaluating possible functional diversity in their seed dispersal kernels. 3. We measured dispersal distances using colour-coded seed mimics embedded in experimental fruits that were offered to the carnivores in feeding stations (simulating source trees). The exclusive colour code of each simulated tree allowed us to assign the exact origin of seed mimics found later in carnivore faeces. We further designed an explicit sampling strategy aiming to detect the longest dispersal events; as far we know, the most robust sampling scheme followed for tracking carnivore-dispersed seeds. 4. We found a marked functional heterogeneity among both species in their seed dispersal kernels according to their home range size: multimodality and long-distance dispersal in the case of the fox and unimodality and short-distance dispersal in the case of the marten (maximum distances = 2846 and 1233 m, respectively). As a consequence, emergent kernels at the guild level (overall and in two different years) were highly dependent on the relative contribution of each carnivore species. 5. Our results provide the first empirical evidence of functional diversity among seed dispersal kernels generated by carnivorous mammals. Moreover, they illustrate for the first time how seed dispersal kernels strongly depend on the relative contribution of different disperser species, thus on the composition of local disperser assemblages. These findings provide a key starting point for understanding and modelling plant population processes that include mammal-mediated seed dispersal, such as connectivity, range expansion and colonization.

Frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes: a multi-scale approach.

BACKGROUND: Knowledge about how frugivory and seed deposition are spatially distributed is valuable to understand the role of dispersers on the structure and dynamics of plant populations. This may be particularly important within anthropogenic areas, where either the patchy distribution of wild plants or the presence of cultivated fleshy-fruits may influence plant-disperser interactions. METHODOLOGY/PRINCIPAL FINDINGS: We investigated frugivory and spatial patterns of seed deposition by carnivorous mammals in anthropogenic landscapes considering two spatial scales: 'landscape' (∼10 km(2)) and 'habitat type' (∼1-2 km(2)). We sampled carnivore faeces and plant abundance at three contrasting habitats (chestnut woods, mosaics and scrublands), each replicated within three different landscapes. Sixty-five percent of faeces collected (n = 1077) contained seeds, among which wild and cultivated seeds appeared in similar proportions (58% and 53%) despite that cultivated fruiting plants were much less abundant. Seed deposition was spatially structured among both spatial scales being different between fruit types. Whereas the most important source of spatial variation in deposition of wild seeds was the landscape scale, it was the habitat scale for cultivated seeds. At the habitat scale, seeds of wild species were mostly deposited within mosaics while seeds of cultivated species were within chestnut woods and scrublands. Spatial concordance between seed deposition and plant abundance was found only for wild species. CONCLUSIONS/SIGNIFICANCE: Spatial patterns of seed deposition by carnivores differed between fruit types and seemed to be modulated by the fleshy-fruited plant assemblages and the behaviour of dispersers. Our results suggest that a strong preference for cultivated fruits by carnivores may influence their spatial foraging behaviour and lower their dispersal services to wild species. However, the high amount of seeds removed within and between habitats suggests that carnivores must play an important role--often overlooked--as 'restorers' and 'habitat shapers' in anthropogenic areas.

Importance of canine distemper virus (CDV) infection in free-ranging Iberian lynxes (Lynx pardinus).

Canine distemper virus (CDV) is a morbillivirus that is the etiological agent of one of the most important viral diseases affecting canids and an expanding range of other carnivores. Using real-time RT-PCR, CDV RNA was detected in organs of an Iberian lynx (Lynx pardinus) found dead in the Doñana National Park, Southwestern Andalusia, Spain. This finding may be of great importance for the conservation of the species; at present the Iberian lynx is the most critically endangered wild felid. The aim of the present study was to elucidate the significance of CDV for the Iberian lynx population. High viral loads were evident in the dead lynx, suggesting an etiological involvement of CDV in its death. When carnivores from the same region were analyzed by CDV RT-PCR, a stone marten (Martes foina) was positive. Phylogenetic analyses demonstrated high identity of the two detected CDVs and a close relationship to the European dog lineage of CDV. Antibodies to CDV were detected in 14.8% of 88 tested free-ranging Iberian lynxes. The sample seroprevalence was significantly higher in lynxes from the Doñana Natural Space (22.9%) than Sierra Morena (5%). The stone marten and a red fox (Vulpes vulpes) also tested seropositive. In conclusion, CDV is present in the Iberian lynx population, especially in the Doñana region, with sporadic cases of disease. To reduce the infectious pressure of CDV on this endangered population, a mass dog vaccination should be considered.

Feline leukemia virus infection: a threat for the survival of the critically endangered Iberian lynx (Lynx pardinus).

The Iberian lynx (Lynx pardinus) is considered the most endangered felid species in the world. To date, less than 200 animals remain in the wild. Low numbers and genetic uniformity may contribute to render this species particularly susceptible to infectious diseases. Different pathogens have been identified in Iberian lynxes; including several feline bacterial and viral agents. Within a 6-month period starting in December 2006, 12 lynxes living in the northern part of the Doñana area were found to be infected with feline leukemia virus (FeLV). Eleven of these animals were antigenemic, and four of them died in the wild in less than 6 months since the first infected animal had been discovered. The remaining viremic lynxes were captured and allocated to a quarantine center to stop the spread of the infection. An additional three animals died shortly in the quarantine center due to acute anemic disease. Sequencing of the envelope surface unit gene revealed a common origin for the FeLV found in all lynxes. The sequences were closely related to FeLV-A/61E, originally isolated from cats in the USA. Our data demonstrate that, similarly to FeLV, the introduction of a new or particularly pathogenic infection brought into the small population of Iberian lynxes by other wild carnivores or feral cats and dogs roaming in the same habitats have severe consequences. It could result in epidemics that have the potential to eradicate the entire lynx population.

Competitive asymmetries in the use of supplementary food by the endangered Iberian lynx (Lynx pardinus).

BACKGROUND: As a conservation tool, supplementary feeding programs may be directed to specific individuals or sectors of the target population whose productivity or survival is thought to be limited by food scarcity. However, the use of supplemental food by different sex and age classes has received little attention. We studied individual variation in the access of the endangered Iberian lynx (Lynx pardinus) to supplementary food. METHODOLOGY/PRINCIPAL FINDINGS: From 5349 pictures taken with automatic cameras placed in 25 feeding stations, we identified 28 individuals whose sex and age were known. All individuals known to live in areas subjected to supplementation regularly visited feeding stations. Food consumption was not proportional to expected variations in energy demand within sex and age classes. Food consumption by males was higher than by females, and increased with age, in agreement with a despotic distribution. Food consumption also increased with lynx body mass, and this pattern held for individuals sharing the same breeding territories. The access of inferior competitors increased with the number of feeding stations available within lynx territories. CONCLUSIONS/SIGNIFICANCE: All lynx exposed to food supplementation made a regular use of extra food but individuals predicted to be competitively dominant visited stations more frequently than subordinates of the same breeding territory. Our results suggest that insufficient provision of supplementary food could restrict the access of juveniles, or even adult females, to feeding stations. Limited consumption by these target individuals may compromise the efficiency of the supplementary feeding programme at the population level, in endangered species that, as the Iberian lynx, exhibit marked sexual dimorphism in body size.

Feline leukemia virus and other pathogens as important threats to the survival of the critically endangered Iberian lynx (Lynx pardinus).

BACKGROUND: The Iberian lynx (Lynx pardinus) is considered the most endangered felid species in the world. In order to save this species, the Spanish authorities implemented a captive breeding program recruiting lynxes from the wild. In this context, a retrospective survey on prevalence of selected feline pathogens in free-ranging lynxes was initiated. METHODOLOGY/ PRINCIPAL FINDINGS: We systematically analyzed the prevalence and importance of seven viral, one protozoan (Cytauxzoon felis), and several bacterial (e.g., hemotropic mycoplasma) infections in 77 of approximately 200 remaining free-ranging Iberian lynxes of the Doñana and Sierra Morena areas, in Southern Spain, between 2003 and 2007. With the exception of feline immunodeficiency virus (FIV), evidence of infection by all tested feline pathogens was found in Iberian lynxes. Fourteen lynxes were feline leukemia virus (FeLV) provirus-positive; eleven of these were antigenemic (FeLV p27 positive). All 14 animals tested negative for other viral infections. During a six-month period in 2007, six of the provirus-positive antigenemic lynxes died. Infection with FeLV but not with other infectious agents was associated with mortality (p<0.001). Sequencing of the FeLV surface glycoprotein gene revealed a common origin for ten of the eleven samples. The ten sequences were closely related to FeLV-A/61E, originally isolated from cats in the USA. Endogenous FeLV sequences were not detected. CONCLUSIONS/SIGNIFICANCE: It was concluded that the FeLV infection most likely originated from domestic cats invading the lynx's habitats. Data available regarding the time frame, co-infections, and outcome of FeLV-infections suggest that, in contrast to the domestic cat, the FeLV strain affecting the lynxes in 2007 is highly virulent to this species. Our data argue strongly for vaccination of lynxes and domestic cats in and around lynx's habitats in order to prevent further spread of the virus as well as reduction the domestic cat population if the lynx population is to be maintained.