Behaviorally-mediated trophic cascade attenuated by prey use of risky places at safe times.

The mere threat of predation may incite behavioral changes in prey that lead to community-wide impacts on productivity, biodiversity, and nutrient cycling. The paucity of experimental manipulations, however, has contributed to controversy over the strength of this pathway in wide-ranging vertebrate systems. We investigated whether simulated gray wolf (Canis lupus) presence can induce behaviorally-mediated trophic cascades, specifically, whether the 'fear' of wolf olfactory cues alone can change deer foraging behavior in ways that affect plants and soils. Wolves were recently removed from the Cedar Creek Ecosystem Science Reserve (Minnesota, USA), such that consumptively mediated predator effects were negligible. At 32 experimental plots, we crossed two nested treatments: wolf urine application and herbivore exclosures. We deployed camera traps to quantify how white-tailed deer (Odocoileus virginianus) adjusted their spatiotemporal habitat use, foraging, and vigilance in response to wolf cues and how these behavioral changes affected plant productivity, plant communities, and soil nutrients. Weekly applications of wolf urine significantly altered deer behavior, but deer responses did not cascade to affect plant or soil properties. Deer substantially reduced crepuscular activity at wolf-simulated sites compared to control locations. As wolves in this area predominantly hunted during mornings and evenings, this response potentially allows deer to maximize landscape use by accessing dangerous areas when temporal threat is low. Our experiment suggests that prey may be sensitive to 'dynamic' predation risk that is structured across both space and time and, consequentially, prey use of risky areas during safe times may attenuate behaviorally-mediated trophic cascades at the predator-prey interface.

Seasonal Cycles in Hematology and Body Mass in Free-Ranging Gray Wolves (Canis lupus) from Northeastern Minnesota, USA.

Studies of captive gray wolves (Canis lupus) showed seasonal cycles in hematologic values and female body mass. We used a remotely controlled recapture collar to determine whether nine female and five male free-ranging wolves handled four to 17 times in NE Minnesota, US showed similar cycles. Hematocrit, hemoglobin, red blood cell count, mean corpuscular hemoglobin, mean corpuscular hemoglobin concentration, and body mass increased from summer toward a winter peak and then decreased again toward summer. Several hematologic values differed considerably from those of captive wolves, and the ranges in free-ranging wolves were much greater than those of captives.

Studies of wolf x coyote hybridization via artificial insemination.

Following the production of western gray wolf (Canis lupus) x western coyote (Canis latrans) hybrids via artificial insemination (AI), the present article documents that the hybrids survived in captivity for at least 4 years and successfully bred with each other. It further reports that backcrossing one of the hybrids to a male gray wolf by AI also resulted in the birth of live pups that have survived for at least 10 months. All male hybrids (F1 and F2) produced sperm by about 10 months of age, and sperm quality of the F1 males fell within the fertile range for domestic dogs, but sperm motility and morphology, in particular, were low in F2 males at 10 months but improved in samples taken at 22 months of age. These studies are relevant to a long-standing controversy about the identity of the red wolf (Canis rufus), the existence of a proposed new species (Canis lycaon) of gray wolf, and to the role of hybridization in mammalian evolution.

Sexually dimorphic aggression indicates male gray wolves specialize in pack defense against conspecific groups.

Aggression directed at conspecific groups is common among gregarious, territorial species, and for some species such as gray wolves (Canis lupus) intraspecific strife is the leading cause of natural mortality. Each individual in a group likely has different measures of the costs and benefits associated with a group task, such as an aggressive attack on another group, which can alter motivation and behavior. We observed 292 inter-pack aggressive interactions in Yellowstone National Park between 1 April 1995 and 1 April 2011 (>5300days of observation) in order to determine the role of both sexes, and the influence of pack, age, and other traits on aggression. We recorded the behaviors and characteristics of all individuals present during the interactions (n=534 individuals) and which individuals participated in each step (i.e. chase, attack, kill, flight) of the interaction. Overall, all wolves were more likely to chase rivals if they outnumbered their opponent, suggesting packs accurately assess their opponent's size during encounters and individuals adjust their behavior based on relative pack size. Males were more likely than females to chase rival packs and gray-colored wolves were more aggressive than black-colored wolves. Male wolves and gray-colored wolves also recorded higher cortisol levels than females and black-colored wolves, indicating hormonal support for more intense aggressive behavior. Further, we found a positive correlation between male age and probability of chasing, while age-specific participation for females remained constant. Chasing behavior was influenced by the sex of lone intruders, with males more likely to chase male intruders. This difference in behavior suggests male and female wolves may have different strategies and motivations during inter-pack aggressive interactions related to gray wolf mating systems. A division of labor between pack members concerning resource and territory defense suggests selection for specific traits related to aggression is an adaptive response to intense competition between groups of conspecifics.

A SEROSURVEY OF DISEASES OF FREE-RANGING GRAY WOLVES (CANIS LUPUS) IN MINNESOTA, USA.

We tested serum samples from 387 free-ranging wolves ( Canis lupus ) from 2007 to 2013 for exposure to eight canid pathogens to establish baseline data on disease prevalence and spatial distribution in Minnesota's wolf population. We found high exposure to canine adenoviruses 1 and 2 (88% adults, 45% pups), canine parvovirus (82% adults, 24% pups), and Lyme disease (76% adults, 39% pups). Sixty-six percent of adults and 36% of pups exhibited exposure to the protozoan parasite Neospora caninum . Exposure to arboviruses was confirmed, including West Nile virus (37% adults, 18% pups) and eastern equine encephalitis (3% adults). Exposure rates were lower for canine distemper (19% adults, 5% pups) and heartworm (7% adults, 3% pups). Significant spatial trends were observed in wolves exposed to canine parvovirus and Lyme disease. Serologic data do not confirm clinical disease, but better understanding of disease ecology of wolves can provide valuable insight into wildlife population dynamics and improve management of these species.

Wolf (Canis lupus) Generation Time and Proportion of Current Breeding Females by Age.

Information is sparse about aspects of female wolf (Canis lupus) breeding in the wild, including age of first reproduction, mean age of primiparity, generation time, and proportion of each age that breeds in any given year. We studied these subjects in 86 wolves (113 captures) in the Superior National Forest (SNF), Minnesota (MN), during 1972-2013 where wolves were legally protected for most of the period, and in 159 harvested wolves from throughout MN wolf range during 2012-2014. Breeding status of SNF wolves were assessed via nipple measurements, and wolves from throughout MN wolf range, by placental scars. In the SNF, proportions of currently breeding females (those breeding in the year sampled) ranged from 19% at age 2 to 80% at age 5, and from throughout wolf range, from 33% at age 2 to 100% at age 7. Excluding pups and yearlings, only 33% to 36% of SNF females and 58% of females from throughout MN wolf range bred in any given year. Generation time for SNF wolves was 4.3 years and for MN wolf range, 4.7 years. These findings will be useful in modeling wolf population dynamics and in wolf genetic and dog-domestication studies.

Production of hybrids between western gray wolves and western coyotes.

Using artificial insemination we attempted to produce hybrids between captive, male, western, gray wolves (Canis lupus) and female, western coyotes (Canis latrans) to determine whether their gametes would be compatible and the coyotes could produce and nurture offspring. The results contribute new information to an ongoing controversy over whether the eastern wolf (Canis lycaon) is a valid unique species that could be subject to the U. S. Endangered Species Act. Attempts with transcervically deposited wolf semen into nine coyotes over two breeding seasons yielded three coyote pregnancies. One coyote ate her pups, another produced a resorbed fetus and a dead fetus by C-section, and the third produced seven hybrids, six of which survived. These results show that, although it might be unlikely for male western wolves to successfully produce offspring with female western coyotes under natural conditions, western-gray-wolf sperm are compatible with western-coyote ova and that at least one coyote could produce and nurture hybrid offspring. This finding in turn demonstrates that gamete incompatibility would not have prevented western, gray wolves from inseminating western coyotes and thus producing hybrids with coyote mtDNA, a claim that counters the view that the eastern wolf is a separate species. However, some of the difficulties experienced by the other inseminated coyotes tend to temper that finding and suggest that more experimentation is needed, including determining the behavioral and physical compatibility of western gray wolves copulating with western coyotes. Thus although our study adds new information to the controversy, it does not settle it. Further study is needed to determine whether the putative Canis lycaon is indeed a unique species.

Use of real-time PCR to detect canine parvovirus in feces of free-ranging wolves.

Using real-time PCR, we tested 15 wolf (Canis lupus) feces from the Superior National Forest (SNF), Minnesota, USA, and 191 from Yellowstone National Park (YNP), USA, collected during summer and 13 during winter for canine parvovirus (CPV)-2 DNA. We also tested 20 dog feces for CPV-2 DNA. The PCR assay was 100% sensitive and specific with a minimum detection threshold of 10(4) 50% tissue culture infective dose. Virus was detected in two winter specimens but none of the summer specimens. We suggest applying the technique more broadly especially with winter feces.

Movements of wolves at the northern extreme of the species' range, including during four months of darkness.

Information about wolf (Canis lupus) movements anywhere near the northern extreme of the species' range in the High Arctic (>75°N latitude) are lacking. There, wolves prey primarily on muskoxen (Ovibos moschatus) and must survive 4 months of 24 hr/day winter darkness and temperatures reaching -53 C. The extent to which wolves remain active and prey on muskoxen during the dark period are unknown, for the closest area where information is available about winter wolf movements is >2,250 km south. We studied a pack of ≥20 wolves on Ellesmere Island, Nunavut, Canada (80°N latitude) from July 2009 through mid-April 2010 by collaring a lead wolf with a Global Positioning System (GPS)/Argos radio collar. The collar recorded the wolf's precise locations at 6:00 a.m. and 6:00 p.m. daily and transmitted the locations by satellite to our email. Straight-line distances between consecutive 12-hr locations varied between 0 and 76 km. Mean (SE) linear distance between consecutive locations (n = 554) was 11 (0.5) km. Total minimum distance traveled was 5,979 km, and total area covered was 6,640 km(2), the largest wolf range reported. The wolf and presumably his pack once made a 263-km (straight-line distance) foray to the southeast during 19-28 January 2010, returning 29 January to 1 February at an average of 41 km/day straight-line distances between 12-hr locations. This study produced the first detailed movement information about any large mammal in the High Arctic, and the average movements during the dark period did not differ from those afterwards. Wolf movements during the dark period in the highest latitudes match those of the other seasons and generally those of wolves in lower latitudes, and, at least with the gross movements measurable by our methods, the 4-month period without direct sunlight produced little change in movements.

A serological survey of infectious disease in Yellowstone National Park's canid community.

BACKGROUND: Gray wolves (Canis lupus) were reintroduced into Yellowstone National Park (YNP) after a >70 year absence, and as part of recovery efforts, the population has been closely monitored. In 1999 and 2005, pup survival was significantly reduced, suggestive of disease outbreaks. METHODOLOGY/PRINCIPAL FINDINGS: We analyzed sympatric wolf, coyote (Canis latrans), and red fox (Vulpes vulpes) serologic data from YNP, spanning 1991-2007, to identify long-term patterns of pathogen exposure, identify associated risk factors, and examine evidence for disease-induced mortality among wolves for which there were survival data. We found high, constant exposure to canine parvovirus (wolf seroprevalence: 100%; coyote: 94%), canine adenovirus-1 (wolf pups [0.5-0.9 yr]: 91%, adults [>or=1 yr]: 96%; coyote juveniles [0.5-1.5 yrs]: 18%, adults [>or=1.6 yrs]: 83%), and canine herpesvirus (wolf: 87%; coyote juveniles: 23%, young adults [1.6-4.9 yrs]: 51%, old adults [>or=5 yrs]: 87%) suggesting that these pathogens were enzootic within YNP wolves and coyotes. An average of 50% of wolves exhibited exposure to the protozoan parasite, Neospora caninum, although individuals' odds of exposure tended to increase with age and was temporally variable. Wolf, coyote, and fox exposure to canine distemper virus (CDV) was temporally variable, with evidence for distinct multi-host outbreaks in 1999 and 2005, and perhaps a smaller, isolated outbreak among wolves in the interior of YNP in 2002. The years of high wolf-pup mortality in 1999 and 2005 in the northern region of the park were correlated with peaks in CDV seroprevalence, suggesting that CDV contributed to the observed mortality. CONCLUSIONS/SIGNIFICANCE: Of the pathogens we examined, none appear to jeopardize the long-term population of canids in YNP. However, CDV appears capable of causing short-term population declines. Additional information on how and where CDV is maintained and the frequency with which future epizootics might be expected might be useful for future management of the Northern Rocky Mountain wolf population.

Predatory senescence in ageing wolves.

It is well established that ageing handicaps the ability of prey to escape predators, yet surprisingly little is known about how ageing affects the ability of predators to catch prey. Research into long-lived predators has assumed that adults have uniform impacts on prey regardless of age. Here we use longitudinal data from repeated observations of individually-known wolves (Canis lupus) hunting elk (Cervus elaphus) in Yellowstone National Park to demonstrate that adult predatory performance declines with age and that an increasing ratio of senescent individuals in the wolf population depresses the rate of prey offtake. Because this ratio fluctuates independently of population size, predatory senescence may cause wolf populations of equal size but different age structure to have different impacts on prey populations. These findings suggest that predatory senescence is an important, though overlooked, factor affecting predator-prey dynamics.

Body size and predatory performance in wolves: is bigger better?

1. Large body size hinders locomotor performance in ways that may lead to trade-offs in predator foraging ability that limit the net predatory benefit of larger size. For example, size-related improvements in handling prey may come at the expense of pursuing prey and thus negate any enhancement in overall predatory performance due to increasing size. 2. This hypothesis was tested with longitudinal data from repeated observations of 94 individually known wolves (Canis lupus) hunting elk (Cervus elaphus) in Yellowstone National Park, USA. Wolf size was estimated from an individually based sex-specific growth model derived from body mass measurements of 304 wolves. 3. Larger size granted individual wolves a net predatory advantage despite substantial variation in its effect on the performance of different predatory tasks; larger size improved performance of a strength-related task (grappling and subduing elk) but failed to improve performance of a locomotor-related task (selecting an elk from a group) for wolves > 39 kg. 4. Sexual dimorphism in wolf size also explained why males outperformed females in each of the three tasks considered (attacking, selecting, and killing). 5. These findings support the generalization that bigger predators are overall better hunters, but they also indicate that increasing size ultimately limits elements of predatory behaviour that require superior locomotor performance. We argue that this could potentially narrow the dietary niche of larger carnivores as well as limit the evolution of larger size if prey are substantially more difficult to pursue than to handle.

Demographic effects of canine parvovirus on a free-ranging wolf population over 30 years.

We followed the course of canine parvovirus (CPV) antibody prevalence in a subpopulation of wolves (Canis lupus) in northeastern Minnesota from 1973, when antibodies were first detected, through 2004. Annual early pup survival was reduced by 70%, and wolf population change was related to CPV antibody prevalence. In the greater Minnesota population of 3,000 wolves, pup survival was reduced by 40-60%. This reduction limited the Minnesota wolf population rate of increase to about 4% per year compared with increases of 16-58% in other populations. Because it is young wolves that disperse, reduced pup survival may have caused reduced dispersal and reduced recolonization of new range in Minnesota.

INTROGRESSION OF COYOTE MITOCHONDRIAL DNA INTO SYMPATRIC NORTH AMERICAN GRAY WOLF POPULATIONS.

Mitochondrial DNA (mtDNA) genotypes of gray wolves and coyotes from localities throughout North America were determined using restriction fragment length polymorphisms. Of the 13 genotypes found among the wolves, 7 are clearly of coyote origin, indicating that genetic transfer of coyote mtDNA into wolf populations has occurred through hybridization. The transfer of mtDNA appears unidirectional from coyotes into wolves because no coyotes sampled have a wolf-derived mtDNA genotype. Wolves possessing coyote-derived genotypes are confined to a contiguous geographic region in Minnesota, Ontario, and Quebec, and the frequency of coyote-type mtDNA in these wolf populations is high (>50%). The ecological history of the hybrid zone suggests that hybridization is taking place in regions where coyotes have only recently become abundant following conversion of forests to farmlands. Dispersing male wolves unable to find conspecific mates may be pairing with female coyotes in deforested areas bordering wolf territories. Our results demonstrate that closely related species of mobile terrestrial vertebrates have the potential for extensive genetic exchange when ecological conditions change suddenly.