Non-random sampling measures the occurrence but not the strength of a textbook trophic cascade.

Although sampling the five tallest young aspen in a stand is useful for detecting the occurrence of any aspen recruitment, this technique overestimates the population response of aspen to wolf reintroduction. Our original conclusion that random sampling described a trophic cascade that was weaker than the one described by non-random sampling is unchanged.

Density-dependent habitat selection alters drivers of population distribution in northern Yellowstone elk.

Although it is well established that density dependence drives changes in organismal abundance over time, relatively little is known about how density dependence affects variation in abundance over space. We tested the hypothesis that spatial trade-offs between food and safety can change the drivers of population distribution, caused by opposing patterns of density-dependent habitat selection (DDHS) that are predicted by the multidimensional ideal free distribution. We addressed this using winter aerial survey data of northern Yellowstone elk (Cervus canadensis) spanning four decades. Supporting our hypothesis, we found positive DDHS for food (herbaceous biomass) and negative DDHS for safety (openness and roughness), such that the primary driver of habitat selection switched from food to safety as elk density decreased from 9.3 to 2.0 elk/km2 . Our results demonstrate how population density can drive landscape-level shifts in population distribution, confounding habitat selection inference and prediction and potentially affecting community-level interactions.

Disease outbreaks select for mate choice and coat color in wolves.

We know much about pathogen evolution and the emergence of new disease strains, but less about host resistance and how it is signaled to other individuals and subsequently maintained. The cline in frequency of black-coated wolves (Canis lupus) across North America is hypothesized to result from a relationship with canine distemper virus (CDV) outbreaks. We tested this hypothesis using cross-sectional data from wolf populations across North America that vary in the prevalence of CDV and the allele that makes coats black, longitudinal data from Yellowstone National Park, and modeling. We found that the frequency of CDV outbreaks generates fluctuating selection that results in heterozygote advantage that in turn affects the frequency of the black allele, optimal mating behavior, and black wolf cline across the continent.

Examination of the interaction between age-specific predation and chronic disease in the Greater Yellowstone Ecosystem.

Predators may create healthier prey populations by selectively removing diseased individuals. Predators typically prefer some ages of prey over others, which may, or may not, align with those prey ages that are most likely to be diseased. The interaction of age-specific infection and predation has not been previously explored and likely has sizable effects on disease dynamics. We hypothesize that predator cleansing effects will be greater when the disease and predation occur in the same prey age groups. We examine the predator cleansing effect using a model where both vulnerability to predators and pathogen prevalence vary with age. We tailor this model to chronic wasting disease (CWD) in mule deer and elk populations in the Greater Yellowstone Ecosystem, with empirical data from Yellowstone grey wolves and cougars. Model results suggest that under moderate, yet realistic, predation pressure from cougars and wolves independently, predators may decrease CWD outbreak size substantially and delay the accumulation of symptomatic deer and elk. The magnitude of this effect is driven by the ability of predators to selectively remove late-stage CWD infections that are likely the most responsible for transmission, but this may not be the age class they typically select. Thus, predators that select for infected young adults over uninfected juveniles have a stronger cleansing effect, and these effects are strengthened when transmission rates increase with increasing prey morbidity. There are also trade-offs from a management perspective-that is, increasing predator kill rates can result in opposing forces on prey abundance and CWD prevalence. Our modelling exploration shows that predators have the potential to reduce prevalence in prey populations when prey age and disease severity are considered, yet the strength of this effect is influenced by predators' selection for demography or body condition. Current CWD management focuses on increasing cervid hunting as the primary management tool, and our results suggest predators may also be a useful tool under certain conditions, but not necessarily without additional impacts on host abundance and demography. Protected areas with predator populations will play a large role in informing the debate over predator impacts on disease.

Sampling bias exaggerates a textbook example of a trophic cascade.

Understanding trophic cascades in terrestrial wildlife communities is a major challenge because these systems are difficult to sample properly. We show how a tradition of non-random sampling has confounded this understanding in a textbook system (Yellowstone National Park) where carnivore [Canis lupus (wolf)] recovery is associated with a trophic cascade involving changes in herbivore [Cervus canadensis (elk)] behaviour and density that promote plant regeneration. Long-term data indicate a practice of sampling only the tallest young plants overestimated regeneration of overstory aspen (Populus tremuloides) by a factor of 4-7 compared to random sampling because it favoured plants taller than the preferred browsing height of elk and overlooked non-regenerating aspen stands. Random sampling described a trophic cascade, but it was weaker than the one that non-random sampling described. Our findings highlight the critical importance of basic sampling principles (e.g. randomisation) for achieving an accurate understanding of trophic cascades in terrestrial wildlife systems.

Patterns and processes of pathogen exposure in gray wolves across North America.

The presence of many pathogens varies in a predictable manner with latitude, with infections decreasing from the equator towards the poles. We investigated the geographic trends of pathogens infecting a widely distributed carnivore: the gray wolf (Canis lupus). Specifically, we investigated which variables best explain and predict geographic trends in seroprevalence across North American wolf populations and the implications of the underlying mechanisms. We compiled a large serological dataset of nearly 2000 wolves from 17 study areas, spanning 80° longitude and 50° latitude. Generalized linear mixed models were constructed to predict the probability of seropositivity of four important pathogens: canine adenovirus, herpesvirus, parvovirus, and distemper virus-and two parasites: Neospora caninum and Toxoplasma gondii. Canine adenovirus and herpesvirus were the most widely distributed pathogens, whereas N. caninum was relatively uncommon. Canine parvovirus and distemper had high annual variation, with western populations experiencing more frequent outbreaks than eastern populations. Seroprevalence of all infections increased as wolves aged, and denser wolf populations had a greater risk of exposure. Probability of exposure was positively correlated with human density, suggesting that dogs and synanthropic animals may be important pathogen reservoirs. Pathogen exposure did not appear to follow a latitudinal gradient, with the exception of N. caninum. Instead, clustered study areas were more similar: wolves from the Great Lakes region had lower odds of exposure to the viruses, but higher odds of exposure to N. caninum and T. gondii; the opposite was true for wolves from the central Rocky Mountains. Overall, mechanistic predictors were more informative of seroprevalence trends than latitude and longitude. Individual host characteristics as well as inherent features of ecosystems determined pathogen exposure risk on a large scale. This work emphasizes the importance of biogeographic wildlife surveillance, and we expound upon avenues of future research of cross-species transmission, spillover, and spatial variation in pathogen infection.

Investigating the Dynamics of Elk Population Size and Body Mass in a Seasonal Environment Using a Mechanistic Integral Projection Model.

Environmentally mediated changes in body size often underlie population responses to environmental change, yet this is not a universal phenomenon. Understanding when phenotypic change underlies population responses to environmental change is important for obtaining insights and robust predictions of population dynamics in a changing world. We develop a dynamic integral projection model that mechanistically links environmental conditions to demographic rates and phenotypic traits (body size) via changes in resource availability and individual energetics. We apply the model to the northern Yellowstone elk population and explore population responses to changing patterns of seasonality, incorporating the interdependence of growth, demography, and density-dependent processes operating through population feedback on available resources. We found that small changes in body size distributions can have large impacts on population dynamics but need not cause population responses to environmental change. Environmental changes that altered demographic rates directly, via increasing or decreasing resource availability, led to large population impacts in the absence of substantial changes to body size distributions. In contrast, environmentally driven shifts in body size distributions could occur with little consequence for population dynamics when the effect of environmental change on resource availability was small and seasonally restricted and when strong density-dependent processes counteracted expected population responses. These findings highlight that a robust understanding of how associations between body size and demography influence population responses to environmental change will require knowledge of the shape of the relationship between phenotypic distributions and vital rates, the population status with regard to its carrying capacity, and importantly the nature of the environmentally driven change in body size and carrying capacity.

Weak spatiotemporal response of prey to predation risk in a freely interacting system.

The extent to which prey space use actively minimizes predation risk continues to ignite controversy. Methodological reasons that have hindered consensus include inconsistent measurements of predation risk, biased spatiotemporal scales at which responses are measured and lack of robust null expectations. We addressed all three challenges in a comprehensive analysis of the spatiotemporal responses of adult female elk (Cervus elaphus) to the risk of predation by wolves (Canis lupus) during winter in northern Yellowstone, USA. We quantified spatial overlap between the winter home ranges of GPS-collared elk and three measures of predation risk: the intensity of wolf space use, the distribution of wolf-killed elk and vegetation openness. We also assessed whether elk varied their use of areas characterized by more or less predation risk across hours of the day, and estimated encounter rates between simultaneous elk and wolf pack trajectories. We determined whether observed values were significantly lower than expected if elk movements were random with reference to predation risk using a null model approach. Although a small proportion of elk did show a tendency to minimize use of open vegetation at specific times of the day, overall we highlight a notable absence of spatiotemporal response by female elk to the risk of predation posed by wolves in northern Yellowstone. Our results suggest that predator-prey interactions may not always result in strong spatiotemporal patterns of avoidance.

Do prey select for vacant hunting domains to minimize a multi-predator threat?

Many ecosystems contain sympatric predator species that hunt in different places and times. We tested whether this provides vacant hunting domains, places and times where and when predators are least active, that prey use to minimize threats from multiple predators simultaneously. We measured how northern Yellowstone elk (Cervus elaphus) responded to wolves (Canis lupus) and cougars (Puma concolor), and found that elk selected for areas outside the high-risk domains of both predators consistent with the vacant domain hypothesis. This enabled elk to avoid one predator without necessarily increasing its exposure to the other. Our results demonstrate how the diel cycle can serve as a key axis of the predator hunting domain that prey exploit to manage predation risk from multiple sources. We argue that a multi-predator, spatiotemporal framework is vital to understand the causes and consequences of prey spatial response to predation risk in environments with more than one predator.

Predation shapes the evolutionary traits of cervid weapons.

Sexually selected weapons evolved to maximize the individual reproductive success of males in many polygynous breeding species. Many weapons are also retained outside of reproductive periods for secondary reasons, but the importance of these secondary functions is poorly understood. Here we leveraged a unique opportunity from the predator-prey system in northern Yellowstone National Park, WY, USA to evaluate whether predation by a widespread, coursing predator (wolves) has influenced a specific weapon trait (antler retention time) in their primary cervid prey (elk). Male elk face a trade-off: individuals casting antlers early begin regrowth before other males, resulting in relatively larger antlers the following year, and thus greater reproductive success, as indicated by research with red deer. We show, however, that male elk that cast their antlers early are preferentially hunted and killed by wolves, despite early casters being in better nutritional condition than antlered individuals. Our results run counter to classic expectations of coursing predators preferring poorer-conditioned individuals, and in so doing, reveal an important secondary function for an exaggerated sexually selected weapon-predatory deterrence. We suggest this secondary function played a key evolutionary role in elk; uniquely among North American cervids, they retain their antlers long after they fulfil their primary role in reproduction.

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.

Competition between apex predators? Brown bears decrease wolf kill rate on two continents.

Trophic interactions are a fundamental topic in ecology, but we know little about how competition between apex predators affects predation, the mechanism driving top-down forcing in ecosystems. We used long-term datasets from Scandinavia (Europe) and Yellowstone National Park (North America) to evaluate how grey wolf (Canis lupus) kill rate was affected by a sympatric apex predator, the brown bear (Ursus arctos). We used kill interval (i.e. the number of days between consecutive ungulate kills) as a proxy of kill rate. Although brown bears can monopolize wolf kills, we found no support in either study system for the common assumption that they cause wolves to kill more often. On the contrary, our results showed the opposite effect. In Scandinavia, wolf packs sympatric with brown bears killed less often than allopatric packs during both spring (after bear den emergence) and summer. Similarly, the presence of bears at wolf-killed ungulates was associated with wolves killing less often during summer in Yellowstone. The consistency in results between the two systems suggests that brown bear presence actually reduces wolf kill rate. Our results suggest that the influence of predation on lower trophic levels may depend on the composition of predator communities.

Influence of group size on the success of wolves hunting bison.

An intriguing aspect of social foraging behaviour is that large groups are often no better at capturing prey than are small groups, a pattern that has been attributed to diminished cooperation (i.e., free riding) in large groups. Although this suggests the formation of large groups is unrelated to prey capture, little is known about cooperation in large groups that hunt hard-to-catch prey. Here, we used direct observations of Yellowstone wolves (Canis lupus) hunting their most formidable prey, bison (Bison bison), to test the hypothesis that large groups are more cooperative when hunting difficult prey. We quantified the relationship between capture success and wolf group size, and compared it to previously reported results for Yellowstone wolves hunting elk (Cervus elaphus), a prey that was, on average, 3 times easier to capture than bison. Whereas improvement in elk capture success levelled off at 2-6 wolves, bison capture success levelled off at 9-13 wolves with evidence that it continued to increase beyond 13 wolves. These results are consistent with the hypothesis that hunters in large groups are more cooperative when hunting more formidable prey. Improved ability to capture formidable prey could therefore promote the formation and maintenance of large predator groups, particularly among predators that specialize on such prey.

Density-dependent intraspecific aggression regulates survival in northern Yellowstone wolves (Canis lupus).

Understanding the population dynamics of top-predators is essential to assess their impact on ecosystems and to guide their management. Key to this understanding is identifying the mechanisms regulating vital rates. Determining the influence of density on survival is necessary to understand the extent to which human-caused mortality is compensatory or additive. In wolves (Canis lupus), empirical evidence for density-dependent survival is lacking. Dispersal is considered the principal way in which wolves adjust their numbers to prey supply or compensate for human exploitation. However, studies to date have primarily focused on exploited wolf populations, in which density-dependent mechanisms are likely weak due to artificially low wolf densities. Using 13 years of data on 280 collared wolves in Yellowstone National Park, we assessed the effect of wolf density, prey abundance and population structure, as well as winter severity, on age-specific survival in two areas (prey-rich vs. prey-poor) of the national park. We further analysed cause-specific mortality and explored the factors driving intraspecific aggression in the prey-rich northern area of the park. Overall, survival rates decreased during the study. In northern Yellowstone, density dependence regulated adult survival through an increase in intraspecific aggression, independent of prey availability. In the interior of the park, adult survival was less variable and density-independent, despite reduced prey availability. There was no effect of prey population structure in northern Yellowstone, or of winter severity in either area. Survival was similar among yearlings and adults, but lower for adults older than 6 years. Our results indicate that density-dependent intraspecific aggression is a major driver of adult wolf survival in northern Yellowstone, suggesting intrinsic density-dependent mechanisms have the potential to regulate wolf populations at high ungulate densities. When low prey availability or high removal rates maintain wolves at lower densities, limited inter-pack interactions may prevent density-dependent survival, consistent with our findings in the interior of the park.

The adaptive value of morphological, behavioural and life-history traits in reproductive female wolves.

Reproduction in social organisms is shaped by numerous morphological, behavioural and life-history traits such as body size, cooperative breeding and age of reproduction, respectively. Little is known, however, about the relative influence of these different types of traits on reproduction, particularly in the context of environmental conditions that determine their adaptive value. Here, we use 14 years of data from a long-term study of wolves (Canis lupus) in Yellowstone National Park, USA, to evaluate the relative effects of different traits and ecological factors on the reproductive performance (litter size and survival) of breeding females. At the individual level, litter size and survival improved with body mass and declined with age (c. 4-5 years). Grey-coloured females had more surviving pups than black females, which likely contributed to the maintenance of coat colour polymorphism in this system. The effect of pack size on reproductive performance was nonlinear as litter size peaked at eight wolves and then declined, and litter survival increased rapidly up to three wolves, beyond which it increased more gradually. At the population level, litter size and survival decreased with increasing wolf population size and canine distemper outbreaks. The relative influence of these different-level factors on wolf reproductive success followed individual > group > population. Body mass was the primary determinant of litter size, followed by pack size and population size. Body mass was also the main driver of litter survival, followed by pack size and disease. Reproductive gains because of larger body size and cooperative breeding may mitigate reproductive losses because of negative density dependence and disease. These findings highlight the adaptive value of large body size and sociality in promoting individual fitness in stochastic and competitive environments.

Modeling effects of environmental change on wolf population dynamics, trait evolution, and life history.

Environmental change has been observed to generate simultaneous responses in population dynamics, life history, gene frequencies, and morphology in a number of species. But how common are such eco-evolutionary responses to environmental change likely to be? Are they inevitable, or do they require a specific type of change? Can we accurately predict eco-evolutionary responses? We address these questions using theory and data from the study of Yellowstone wolves. We show that environmental change is expected to generate eco-evolutionary change, that changes in the average environment will affect wolves to a greater extent than changes in how variable it is, and that accurate prediction of the consequences of environmental change will probably prove elusive.

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.