Vicuña antipredator diel movement drives spatial nutrient subsidies in a high Andean ecosystem.

Large animals could be important drivers of spatial nutrient subsidies when they ingest resources in some habitats and release them in others, even moving nutrients against elevational gradients. In high Andean deserts, vicuñas (Vicugna vicugna) move daily between nutrient-rich wet meadows, where there is abundant water and forage but high risk of predation by pumas (Puma concolor), and nutrient-poor open plains with lower risk of predation. In all habitats, vicuñas defecate and urinate in communal latrines. We investigated how these latrines impacted soil and plant nutrient concentrations across three habitats in the Andean ecosystem (meadows, plains, and canyons) and used stable isotope analysis to explore the source of fecal nutrients in latrines. Latrine soils had higher concentrations of nitrogen, carbon, and other nutrients than did nonlatrine soils across all habitats. These inputs corresponded with an increase in plant quality (lower C:N) at latrine sites in plains and canyons, but not in meadows. Stable isotope mixing models suggest that ~7% of nutrients in plains latrines originated from vegetation in meadows, which is disproportionately higher than the relative proportion of meadow habitat (2.6%) in the study area. In contrast, ~68% of nutrients in meadow latrines appear to originate from plains and canyon vegetation, though these habitats made up nearly 98% of the study area. Vicuña diel movements thus appear to concentrate nutrients in latrines within habitats and to drive cross-habitat nutrient subsidies, with disproportionate transport from low-lying, nutrient-rich meadows to more elevated, nutrient-poor plains. When these results are scaled up to the landscape scale, the amount of nitrogen and phosphorus subsidized in soil at plains latrines was of the same order of magnitude as estimates of annual atmospheric nitrogen and phosphorus deposition for this region (albeit far more localized and patchy). Thus, vicuña-mediated nutrient redistribution and deposition appears to be an important process impacting ecosystem functioning in arid Andean environments, on par with other major inputs of nutrients to the system.

Spatial ecology of the Vicuña (Lama vicugna) in a high Andean protected area.

The study of animal space use is fundamental to effective conservation and management of wildlife populations and habitats in a rapidly changing world, yet many species remain poorly described. Such is the case for the spatial ecology of the Vicuña-a medium-sized wild camelid that plays a critical role, both as a consumer and as prey, in the high Andean food web. We studied patterns of space use of 24 adult female vicuñas from April 2014 to February 2017 at the southern edge of its range. Vicuñas showed strong fidelity to their home range locations across the study period and shared large portions of their home ranges with vicuñas from other family groups. Vicuña home ranges in our study were considerably larger than previous estimates across the range of the species. Variation in environmental and terrain factors and the associated risk of predation affected vicuña diel migration distance but not home range size or overlap. Our study offers new ecological insights into vicuña space use that can inform conservation and management efforts of vicuñas and other social ungulates.

El estudio del uso del espacio en animales es fundamental para la conservación y gestión eficaz de sus poblaciones y hábitats silvestres en un mundo que cambia rápidamente, sin embargo muchas especies siguen estando mal descritas. Tal es el caso del estudio de ecología espacial de la vicuña, un camélido silvestre de tamaño mediano que tiene un papel crítico en la red trófica altoandina. Estudiamos el uso del espacio de 24 hembras adultas de vicuñas desde abril de 2014 hasta febrero de 2017 en el extremo sur del área de distribución de la especie. Las vicuñas mostraron una gran fidelidad en la ubicación de sus áreas de acción durante el período de estudio y compartieron gran parte de sus áreas de acción con otros grupos familiars. Las áreas de acción de las vicuñas en nuestro estudio fueron considerablemente más grandes que las estimaciones previas en todo el rango de la especie. Variacíon en factores ambientales y topográficos, y el riesgo asociado de depredación afectaron las distancias de las migraciones diarias de las vicuñas, pero no afectaron el tamaño del área de acción. Nuestro estudio reporta nuevos datos ecológicos sobre el uso del espacio de vicuñas que pueden informar los esfuerzos de conservación y manejo de esta especie y otros ungulados sociales.

Risk effects cascade up to an obligate scavenger.

The effects of predation risk on prey populations have been studied extensively; yet, how risk is manifested in a trophically linked guild-scavengers-has been overlooked. Risk could be particularly consequential for obligate scavengers that are vulnerable while foraging and rely on carrion provisioned by, and shared with, apex predators. We investigated whether Andean condors (Vultur gryphus) respond to predation risk in a landscape where the main source of carrion are camelids killed by pumas (Puma concolor). We hypothesized that condors would exhibit different behavioral responses to predation risk while they search, encounter, and exploit carrion. We explored condor habitat selection while flying by tracking nine birds with satellite transmitters and monitored via camera traps 41 natural carcasses and 25 experimental carrion stations. We found that condors searched for carrion in areas with a high probability of occurrence of puma kills. However, condors avoided exploiting carrion in areas featuring tall vegetation and steep slopes-selected by pumas to stalk prey-suggesting that condors manage risk primarily through the identification of safe foraging sites prior to landing. Our finding that condors avoided foraging near stalking cover for pumas highlights the importance of risk effects beyond predator-prey interactions, particularly for obligate scavengers.

Phenological drivers of ungulate migration in South America: characterizing the movement and seasonal habitat use of guanacos.

BACKGROUND: Migration is a widespread strategy among ungulates to cope with seasonality. Phenology, especially in seasonally snow-covered landscapes featuring "white waves" of snow accumulation and "green waves" of plant green-up, is a phenomenon that many migratory ungulates navigate. Guanacos (Lama guanicoe) are native camelids to South America and might be the last ungulate in South America that migrates. However, a detailed description of guanacos´ migratory attributes, including whether they surf or jump phenological waves is lacking. METHODS: We quantified the migratory movements of 21 adult guanacos over three years in Patagonia, Argentina. We analyzed annual movement patterns using net squared displacement (NSD) and home range overlap and quantified snow and vegetation phenology via remotely sensed products. RESULTS: We found that 74% of the individual guanacos exhibited altitudinal migrations. For migratory guanacos, we observed fidelity of migratory ranges and residence time, but flexibility around migration propensity, timing, and duration of migration. The scarce vegetation and arid conditions within our study area seemed to prevent guanacos from surfing green waves; instead, guanacos appeared to avoid white waves. CONCLUSION: Our study shows that guanaco elevational migration is driven by a combination of vegetation availability and snow cover, reveals behavioral plasticity of their migration, and highlights the importance of snow phenology as a driver of ungulate migrations.

Carnivore Niche Partitioning in a Human Landscape.

AbstractTo minimize competitive overlap, carnivores modify one of their critical niche axes: space, time, or resources. However, we currently lack rules for how carnivore communities operate in human-dominated landscapes. We simultaneously quantified overlap in the critical niche axes of a simple carnivore community-an apex carnivore (Puma concolor), a dominant mesocarnivore (Lycalopex culpaeus), and a subordinate small carnivore (Lycalopex griseus)-in a human landscape featuring pastoralists and semidomestic carnivores (i.e., dogs, Canis familiaris). We found that dominant species had strong negative effects on the space use of subordinate ones, which ultimately created space for subordinate small carnivores. Humans and dogs were strictly diurnal, whereas the native carnivore community was nocturnal and exhibited high temporal overlap. Dietary overlap was high among the native carnivores, but dogs were trophically decoupled, largely because of human food subsidies. Our results show that in landscapes with evident human presence, temporal and dietary partitioning among native carnivores can be limited, leaving space as the most important axis to be partitioned among carnivores. We believe that these findings-the first to simultaneously assess all three critical niche axes among competing carnivores and humans and their associated species (i.e., domesticated carnivores)-are transferable to other carnivore communities in human-modified landscapes.

Cascading effects of a disease outbreak in a remote protected area.

Disease outbreaks induced by humans increasingly threaten wildlife communities worldwide. Like predators, pathogens can be key top-down forces in ecosystems, initiating trophic cascades that may alter food webs. An outbreak of mange in a remote Andean protected area caused a dramatic population decline in a mammalian herbivore (the vicuña), creating conditions to test the cascading effects of disease on the ecological community. By comparing a suite of ecological measurements to pre-disease baseline records, we demonstrate that mange restructured tightly linked trophic interactions previously driven by a mammalian predator (the puma). Following the mange outbreak, scavenger (Andean condor) occurrence in the ecosystem declined sharply and plant biomass and cover increased dramatically in predation refuges where herbivory was historically concentrated. The evidence shows that a disease-induced trophic cascade, mediated by vicuña density, could supplant the predator-induced trophic cascade, mediated by vicuña behaviour, thereby transforming the Andean ecosystem.

Sarcoptic mange outbreak decimates South American wild camelid populations in San Guillermo National Park, Argentina.

Sarcoptic mange epidemics can devastate wildlife populations. In 2014, mange was first detected in vicuñas (Vicugna vicugna) and guanacos (Lama guanicoe) in San Guillermo National Park (SGNP), Argentina. This study describes the temporal dynamics of the outbreak, its effects on the park's wild camelid populations between 2017-2019, and investigates the potential source of the epidemic. From May 2017 to June 2018, transect surveys indicated a sharp decrease in the density of living vicuñas and guanacos by 68% and 77%, respectively. By April 2019 no vicuñas or guanacos were recorded on transect surveys, suggesting their near-extinction in the park. Clinical signs consistent with mange (e.g., intense scratching, hyperkeratosis, alopecia) were observed in 24% of living vicuñas (n = 478) and 33% of living guanacos (n = 12) during surveys, as well as in 94% of vicuña carcasses (n = 124) and 85% of guanaco carcasses (n = 20) examined. Sarcoptes scabiei was identified as the causal agent by skin scrapings, and the cutaneous lesions were characterized by histopathology (n = 15). Genetic characterization revealed that mites recovered from seven vicuñas (n = 13) and three guanacos (n = 11) shared the same genotype, which is consistent with a single source and recent origin of the epidemic. Tracing the potential source, we identified a governmental livestock incentive program which introduced llamas (Lama glama) in areas adjacent to SGNP in 2009, some of which had alopecic scaling consistent with sarcoptic mange. Though at the time of our study no llamas with mange were available for confirmatory sampling, we hypothesize that the introduction of mange-infected llamas may have triggered the outbreak in wild camelids. This unprecedented event in SGNP had devastating effects on dominating herbivores with potentially profound cascading effects at the community and ecosystem levels.

Where and when to hunt? Decomposing predation success of an ambush carnivore.

Predator-prey games emerge when predators and prey dynamically respond to the behavior of one another, driving the outcomes of predator-prey interactions. Predation success is a function of the combined probabilities of encountering and capturing prey, which are influenced by both prey behavior and environmental features. While the relative importance of encounter and capture probabilities have been evaluated in a spatial framework, temporal variation in prey behavior and intrinsic catchability are likely to also affect the distribution of predation events. Using a single-predator-single-prey (puma-vicuña) system, we evaluated which factors predict predation events across both temporal and spatial dimensions of the components of predation by testing the prey-abundance hypothesis (predators select for high encounter probability) and the prey-catchability hypothesis (predators select for high relative capture probability) in time and space. We found that for both temporal and spatial analyses, neither the prey-abundance hypothesis nor the prey-catchability hypothesis alone predicted kill frequency or distribution; puma kill frequency was static throughout the diel cycle and pumas consistently selected a single habitat type when hunting, despite temporal and spatial variation in encounter rates and intrinsic catchability. Our integrated spatiotemporal analysis revealed that an interaction between time of day and habitat influences kill probability, suggesting that trade-offs in the temporal and spatial components of predation drive the probability of predation events. These findings reinforce the importance of examining both the temporal and spatial patterns of the components of predation, rather than unidimensional measures of predator or prey behavior, to comprehensively describe the feedbacks between predator and prey in the predator-prey game.

Habitat complexity mediates the predator-prey space race.

The spatial relationship between predator and prey is often conceptualized as a behavioral response race, in which prey avoid predators while predators track prey. Limiting habitat types can create spatial anchors for prey or predators, influencing the likelihood that the predator or prey response will dominate. Joint spatial anchors emerge when predator and prey occupy similar feeding habitat domains and risk and reward become spatially conflated, confusing predictions of which player will win the space race. These spatial dynamics of risk-foraging trade-offs are often obscured by habitat heterogeneity and community complexity in large vertebrate systems, fueling ambiguity regarding the generality of predictions from predator-prey theory. To test how habitat distribution influences the predator-prey space race, we examine correlation in puma and vicuña habitat selection and space use at two sites, one of which generates a distinct risk-foraging trade-off at a joint spatial anchor. The distribution of vegetation, which serves as both forage for vicuñas and stalking cover for pumas, differs between the sites; the llano contains a single central meadow that acts as a joint spatial anchor, while the canyon is characterized by more heterogeneous vegetation. Puma-vicuña habitat selection correlation was positive in the llano and negative in the canyon, and similarly, utilization distributions were more strongly correlated in the llano than the canyon. Vicuña locations occurred at higher values of puma habitat selection and utilization in the llano than in the canyon. Similarly, puma locations in the llano occurred at higher values of vicuña habitat selection and utilization than in the canyon. Although pumas consistently selected for and utilized vegetative and topographic cover regardless of habitat distribution, vicuñas only selected against vegetation in the heterogeneous canyon site, reducing spatial correlation with pumas. Our work suggests a joint spatial anchor favors pumas in the space race due to the inability for vicuñas to avoid crucial foraging habitat. The outcome of the predator-prey space race appears to be strongly informed by the distribution of habitat, whereby corresponding predictability of predator and prey favors predators in the spatial game.

Integrating temporal refugia into landscapes of fear: prey exploit predator downtimes to forage in risky places.

The landscape of fear is an important driver of prey space use. However, prey can navigate the landscape of fear by exploiting temporal refuges from predation risk. We hypothesized that diel patterns of predator and prey movement and space use would be inversely correlated due to temporal constraints on predator habitat domain. Specifically, we evaluated habitat selection and activity of the vicuña and its only predator, the puma, during three diel periods: day, dawn/dusk, and night. Pumas selected the same habitats regardless of diel period-vegetated and rugged areas that feature stalking cover for pumas-but increased their activity levels during dawn/dusk and night when they benefit from reduced detection by prey. Vicuñas avoided areas selected by pumas and reduced activity at night, but selected vegetated areas and increased activity by day and dawn/dusk. Vicuña habitat selection and movement strategies appeared to reduce the risk of encountering pumas; movement rates of pumas and vicuñas were negatively correlated across the diel cycle, and habitat selection was negatively correlated during dawn/dusk and night. Our study shows that an ambush predator's temporal activity and space use patterns interact to create diel refugia and shape the antipredator behaviors of its prey. Importantly, it is likely the very nature of ambush predators' static habitat specificity that makes predator activity important to temporally varying perceptions of risk. Prey which depend on risky habitats for foraging appear to mitigate risk by feeding when they can more easily detect predators and when predators are least active.

Diet, morphology, and interspecific killing in carnivora.

Interspecific killing is a key determinant of the abundances and distributions of carnivores, their prey, and nonprey community members. Similarity of body size has been proposed to lead competitors to seek similar prey, which increases the likelihood of interference encounters, including lethal ones. We explored the influence of body size, diet, predatory habits, and taxonomic relatedness on interspecific killing. The frequency of attacks depends on differences in body size: at small and large differences, attacks are less likely to occur; at intermediate differences, killing interactions are frequent and related to diet overlap. Further, the importance of interspecific killing as a mortality factor in the victim population increases with an increase in body size differences between killers and victims. Carnivores highly adapted to kill vertebrate prey are more prone to killing interactions, usually with animals of similar predatory habits. Family-level taxonomy influences killing interactions; carnivores tend to interact more with species in the same family than with species in different families. We conclude that although resource exploitation (diet), predatory habits, and taxonomy are influential in predisposing carnivores to attack each other, relative body size of the participants is overwhelmingly important. We discuss the implications of interspecific killing for body size and the dynamics of geographic ranges.