Heiko U. Wittmer

The role of predation in the decline and extirpation of woodland caribou

To select appropriate recovery strategies for endangered populations, we must understand the dynamics of small populations and distinguish between the possible causes that drive such populations to low numbers. It has been suggested that the pattern of population decline may be inversely density-dependent with population growth rates decreasing as populations become very small; however, empirical evidence of such accelerated declines at low densities is rare. Here we analyzed the pattern of decline of a threatened population of woodland caribou (Rangifer tarandus caribou) in British Columbia, Canada. Using information on the instantaneous rate of increase relative to caribou density in suitable winter foraging habitat, as well as on pregnancy rates and on causes and temporal distribution of mortalities from a sample of 349 radiocollared animals from 15 subpopulations, we tested 3 hypothesized causes of decline: (a) food regulation caused by loss of suitable winter foraging habitat, (b) predation-sensitive foraging caused by loss of suitable winter foraging habitat and (c) predation with caribou being secondary prey. Population sizes of caribou subpopulations ranged from <5 to >500 individuals. Our results showed that the rates of increase of these subpopulations varied from −0.1871 to 0.0496 with smaller subpopulations declining faster than larger subpopulations. Rates of increase were positively related to the density of caribou in suitable winter foraging habitat. Pregnancy rates averaged 92.4% ±2.24 and did not differ among subpopulations. In addition, we found predation to be the primary cause of mortality in 11 of 13 subpopulations with known causes of mortality and predation predominantly occurred during summer. These results are consistent with predictions that caribou subpopulations are declining as a consequence of increased predation. Recovery of these woodland caribou will thus require a multispecies perspective and an appreciation for the influence of inverse density dependence on population trajectories.

A restricted hybrid zone between native and introduced red fox (Vulpes vulpes) populations suggests reproductive barriers and competitive exclusion.

Introduced species can threaten native taxa in multiple ways, including competition and hybridization, which can reduce fitness, alter ecological niches or swamp native genomes. Encroachment and hybridization by introduced species also provide opportunities to study the dynamics of invasiveness and hybridization during early stages following contact. We used 33 microsatellites, 51 single nucleotide polymorphisms and a mtDNA marker to characterize the extent and spatial pattern of encroachment and hybridization between a native, endemic subspecies of red fox (Vulpes vulpes patwin) and an introduced red fox population composed of highly admixed, phylogenetically divergent stock, resulting from a century of domestication. Both nuclear and mtDNA markers indicated that hybridization was primarily restricted to a narrow zone where the two populations came into contact. Although a few introgressed genotypes were detected in the interior of the native range, we found no immigrant foxes or F1 or F2 hybrids there, suggesting native foxes excluded introduced individuals. We speculate that the observed interbreeding at the periphery was facilitated by low densities. In total, 98% of mtDNA haplotypes in the native range were native and 96% of the nuclear ancestry was estimated to be native. Although the introduced range had expanded fivefold over the past four decades, native and non‐native haplotypes from museum samples collected in and near the native range three decades earlier showed a similar geographic distribution as today, suggesting that the native range and hybrid zone were relatively stable. We hypothesize that the monogamous mating system of red foxes and other wild canids may enhance their resistance to hybridization because of greater fitness consequences associated with mate discrimination.

Incorporating Allee effects into reintroduction strategies

Allee effects, the reduction of vital rates at low population densities, can occur through several mechanisms, all of which potentially apply to reintroduced populations. Reintroduced populations are initially at low densities, hence Allee effects can potentially lead to reintroduction failure despite habitat quality being sufficient to allow long-term persistence if the population survived the establishment phase. The probability of such failures can potentially be reduced by releasing large numbers of organisms, by reducing post-release dispersal or mortality through management, or by directly managing the Allee effects, e.g., by implementing predator control or food supplementation until population size increases. However, such measures incur costs, as large releases have a greater impact on source populations, and management actions require financial and other resources. It is therefore essential to compare the costs and benefits of attempting to reduce Allee effects in reintroduction programs. Here we advocate the use of structured decision-making frameworks whereby alternative strategies are nominated, probability distributions of outcomes obtained under different strategies, and utilities assigned to different outcomes. We illustrate the potential application of such decision frameworks using projections from a stochastic population model including Allee effects. As there will seldom be estimates of Allee effects available from the species or system involved, it will be necessary to predict these effects based on the biology of the species and data from other systems. In doing so, it is important to identify mechanisms for proposed Allee effects, and to avoid misleading inferences from correlations subject to confounds. In particular, naive interpretations of correlations between numbers released and reintroduction success may exaggerate the benefits of releasing large numbers.

Nuisance Ecology: Do Scavenging Condors Exact Foraging Costs on Pumas in Patagonia?

Predation risk describes the energetic cost an animal suffers when making a trade off between maximizing energy intake and minimizing threats to its survival. We tested whether Andean condors (Vultur gryphus) influenced the foraging behaviors of a top predator in Patagonia, the puma (Puma concolor), in ways comparable to direct risks of predation for prey to address three questions: 1) Do condors exact a foraging cost on pumas?; 2) If so, do pumas exhibit behaviors indicative of these risks?; and 3) Do pumas display predictable behaviors associated with prey species foraging in risky environments? Using GPS location data, we located 433 kill sites of 9 pumas and quantified their kill rates. Based upon time pumas spent at a carcass, we quantified handling time. Pumas abandoned >10% of edible meat at 133 of 266 large carcasses after a single night, and did so most often in open grasslands where their carcasses were easily detected by condors. Our data suggested that condors exacted foraging costs on pumas by significantly decreasing puma handling times at carcasses, and that pumas increased their kill rates by 50% relative to those reported for North America to compensate for these losses. Finally, we determined that the relative risks of detection and associated harassment by condors, rather than prey densities, explained puma “giving up times” (GUTs) across structurally variable risk classes in the study area, and that, like many prey species, pumas disproportionately hunted in high-risk, high-resource reward areas.

The Comparative Effects of Large Carnivores on the Acquisition of Carrion by Scavengers

Pumas (Puma concolor) and black bears (Ursus americanus) are large carnivores that may influence scavenger population dynamics. We used motion-triggered video cameras deployed at deer carcasses to determine how pumas and black bears affected three aspects of carrion acquisition by scavengers: presence, total feeding time, and mean feeding-bout duration. We found that pumas were unable to limit acquisition of carrion by large carnivores but did limit aspects of carrion acquisition by both birds and mesocarnivores. Through their suppression of mesocarnivores and birds, pumas apparently initiated a cascading pattern and increased carrion acquisition by small carnivores. In contrast, black bears monopolized carrion resources and generally had larger limiting effects on carrion acquisition by all scavengers. Black bears also limited puma feeding behaviors at puma kills, which may require pumas to compensate for energetic losses through increasing their kill rates of ungulates. Our results suggest that pumas provide carrion and selectively influence species acquiring carrion, while black bears limit carrion availability to all other scavengers. These results suggest that the effects of large carnivores on scavengers depend on attributes of both carnivores and scavengers (including size) and that competition for carcasses may result in intraguild predation as well as mesocarnivore release.

Using Predator-Prey Theory to Predict Outcomes of Broadscale Experiments to Reduce Apparent Competition

Apparent competition is an important process influencing many ecological communities. We used predator-prey theory to predict outcomes of ecosystem experiments aimed at mitigating apparent competition by reducing primary prey. Simulations predicted declines in secondary prey following reductions in primary prey because predators consumed more secondary prey until predator numbers responded to reduced prey densities. Losses were exacerbated by a higher carrying capacity of primary prey and a longer lag time of the predator’s numerical response, but a gradual reduction in primary prey was less detrimental to the secondary prey. We compared predictions against two field experiments where endangered woodland caribou (Rangifer tarandus caribou) were victims of apparent competition. First, when deer (Odocoileus sp.) declined suddenly following a severe winter, cougar (Puma concolor) declined with a 1–2-year lag, yet in the interim more caribou were killed by cougars, and caribou populations declined by 40%. Second, when moose (Alces alces) were gradually reduced using a management experiment, wolf (Canis lupus) populations declined but did not shift consumption to caribou, and the largest caribou subpopulation stabilized. The observed contrasting outcomes of sudden versus gradual declines in primary prey supported theoretical predictions. Combining theory with field studies clarified how to manage communities to mitigate endangerment caused by apparent competition that affects many taxa.

Trophic Facilitation or Limitation? Comparative Effects of Pumas and Black Bears on the Scavenger Community

Scavenging is a widespread behaviour and an important process influencing food webs and ecological communities. Large carnivores facilitate the movement of energy across trophic levels through the scavenging and decomposition of their killed prey, but competition with large carnivores is also likely to constrain acquisition of carrion by scavengers. We used an experimental approach based on motion-triggered video cameras at black-tailed deer (Odocoileus hemionus columbianus) carcasses to measure the comparative influences of two large carnivores in the facilitation and limitation of carrion acquisition by scavengers. We found that pumas (Puma concolor) and black bears (Ursus americanus) had different effects on their ecological communities. Pumas, as a top-level predator, facilitated the consumption of carrion by scavengers, despite significantly reducing their observed sum feeding times (165.7 min±21.2 SE at puma kills 264.3 min±30.1 SE at control carcasses). In contrast, black bears, as the dominant scavenger in the system, limited consumption of carrion by scavengers as evidenced by the observed reduction of scavenger species richness recorded at carcasses where they were present (mean = 2.33±0.28 SE), compared to where they were absent (mean = 3.28±0.23 SE). Black bears also had large negative effects on scavenger sum feeding times (88.5 min±19.8 SE at carcasses where bears were present, 372.3 min±50.0 SE at carcasses where bears were absent). In addition, we found that pumas and black bears both increased the nestedness (a higher level of order among species present) of the scavenger community. Our results suggest that scavengers have species-specific adaptions to exploit carrion despite large carnivores, and that large carnivores influence the structure and composition of scavenger communities. The interactions between large carnivores and scavengers should be considered in future studies of food webs and ecological communities.

The difference between killing and eating: ecological shortcomings of puma energetic models

Bioenergetic modeling is employed to estimate the energetic demands of many cryptic carnivores and their kill rates needed to meet their energetic requirements. We tested two prevalent assumptions driving energetic modeling of predator kill rates: (1) morphological and physiological information (weight, energetic demands of activity patterns) of individual predators are sufficient to accurately predict their kill rates, and (2) kill and consumption rates are equivalent (meaning that carnivores consume all of what they kill). We did this by testing whether two independent energetic models accurately predicted puma (Puma concolor) kill and consumption rates in three study systems in North and South America with variable ecology, including climate and prey assemblages. Our results demonstrated that current puma energetic models drastically underestimate actual puma kill rates quantified through intensive field monitoring. We concluded that puma energetic models more realistically estimate puma consumption rates needed to meet metabolic requirements. Puma kill rates determined from field efforts were not explained by puma weight (in kg) or activity patterns (in distance traveled), which were the variables used in energetic models. Our kill rates in kg/day determined from field investigations of GPS clusters were the highest reported to date and statistically equivalent across three distinct ecosystems, a range of puma characteristics, variable lengths of monitoring, variable daily distances traveled, and across systems with 1–3 ungulate prey. In contrast, puma kill rates in ungulates/week differed across study areas, suggesting that kill rates described in kilograms per day are better suited for comparing puma kill rates across systems while kill rates in terms of ungulates per unit time are better suited for modeling predator-prey dynamics for a particular ecosystem. Based on these results we concluded that energetic models using morphological and physiological variables alone were insufficient to predict kill rates, and proposed that rather than focusing future research on refining current energetic models, future research should be directed at understanding the behavioral ecology driving carnivore kill rates.

Puma communication behaviours: understanding functional use and variation among sex and age classes

Intraspecific communication for mate selection sometimes varies between sexes based on different evolutionary life history patterns. Solitary felids use communication for territorial defence and location of mates, for which they use scent-marking behaviours including scraping, urine spraying, body rubbing, caterwauling, cheek rubbing, and the flehmen response, but these behaviours are not well understood in pumas (Puma concolor). We used motion-triggered video cameras to document the use of communication behaviours by male and female pumas, and used a series of experimental treatments to determine the mechanisms and importance of visual and olfactory cues in puma scrapes. We found that pumas use the physical scrape to locate communications, and then use urine to convey and interpret the communication itself. We also found significant differences among puma age and sex classes in the proportion of use and duration of time behaviours were displayed. Mature males spent significantly longer durations (x = 22.1 s) on producing behaviours (scraping, body rubbing, and caterwauling behaviours) than mature females (x = 3. 3s ), and males used scraping (78.5%) and body rubbing (12.4%) behaviours at a higher proportion of visits than females (13.6 and 2.7%, respectively). Mature females spent significantly longer durations (x = 30.4 s) on consuming behaviours (investigating and flehmen response behaviours) than mature males (x = 13.7 s), and females used flehmen response (30.6%) and caterwauling (9.3%) behaviours at a higher proportion of visits than mature males (6.5% flehmen and 0.4% caterwauling). Male reproductive strategy appears based on advertisement for possible mates, while female reproductive strategy appears based on assessment of possible mates. The use of communication behaviours also appears to develop with age, as immature pumas rarely visited and acted as nonparticipants in communication behaviours.

Table scraps: inter-trophic food provisioning by pumas

Large carnivores perform keystone ecological functions through direct predation, or indirectly, through food subsidies to scavengers or trophic cascades driven by their influence on the distributions of their prey. Pumas (Puma concolor) are an elusive, cryptic species difficult to study and little is known about their inter-trophic-level interactions in natural communities. Using new GPS technology, we discovered that pumas in Patagonia provided 232 ± 31 kg of edible meat/month/100 km2 to near-threatened Andean condors (Vultur gryphus) and other members of a diverse scavenger community. This is up to 3.1 times the contributions by wolves (Canis lupus) to communities in Yellowstone National Park, USA, and highlights the keystone role large, solitary felids play in natural systems. These findings are more pertinent than ever, for managers increasingly advocate controlling pumas and other large felids to bolster prey populations and mitigate concerns over human and livestock safety, without a full understanding of the potential ecological consequences of their actions.