Gary W. Roemer

Golden eagles, feral pigs, and insular carnivores: How exotic species turn native predators into prey

Island ecosystems are particularly vulnerable to exotic species. Here we show how an introduced prey has led to the wholesale restructuring of an island food web, including the near extinction of an endemic carnivore. Introduced pigs, by providing abundant food, enabled golden eagles to colonize the California Channel Islands. Eagles preyed heavily on the island fox, whose resulting decline toward extinction released populations of the competitively inferior island skunk. The presence of exotic pigs led to major ecosystem shifts by indirectly causing predation to replace competition as the dominant force shaping these island communities.

Pleistocene Rewilding: An Optimistic Agenda for Twenty‐First Century Conservation

Large vertebrates are strong interactors in food webs, yet they were lost from most ecosystems after the dispersal of modern humans from Africa and Eurasia. We call for restoration of missing ecological functions and evolutionary potential of lost North American megafauna using extant conspecifics and related taxa. We refer to this restoration as Pleistocene rewilding; it is conceived as carefully managed ecosystem manipulations whereby costs and benefits are objectively addressed on a case‐by‐case and locality‐by‐locality basis. Pleistocene rewilding would deliberately promote large, long‐lived species over pest and weed assemblages, facilitate the persistence and ecological effectiveness of megafauna on a global scale, and broaden the underlying premise of conservation from managing extinction to encompass restoring ecological and evolutionary processes. Pleistocene rewilding can begin immediately with species such as Bolson tortoises and feral horses and continue through the coming decades with elephants and Holarctic lions. Our exemplar taxa would contribute biological, economic, and cultural benefits to North America. Owners of large tracts of private land in the central and western United States could be the first to implement this restoration. Risks of Pleistocene rewilding include the possibility of altered disease ecology and associated human health implications, as well as unexpected ecological and sociopolitical consequences of reintroductions. Establishment of programs to monitor suites of species interactions and their consequences for biodiversity and ecosystem health will be a significant challenge. Secure fencing would be a major economic cost, and social challenges will include acceptance of predation as an overriding natural process and the incorporation of pre‐Columbian ecological frameworks into conservation strategies.

The Ecological Role of the Mammalian Mesocarnivore

Large mammalian carnivores are ecologically important because relatively few individuals can cause strong predation-driven direct effects or fear-driven indirect effects that can ripple through communities and, ultimately, influence ecosystem structure and function. Most mammalian carnivores are not large, however, but are small to midsized species collectively termed “mesocarnivores.” Mesocarnivores are more numerous and more diverse than larger carnivores, and often reside in closer proximity to humans, yet we know little about how they influence communities and ecosystems. In this article we review the ecological role of the mesocarnivore and present examples where mesocarnivores drive community structure and function in roles similar to, or altogether different from, their larger brethren. Together, these examples substantiate the need for an assessment of the ecological role of mammalian carnivores beyond an examination of only the largest species. In particular, we emphasize the need to study the trophic penetrance of mesocarnivores and examine how ecological context modulates their functional role.

Feral pigs facilitate hyperpredation by golden eagles and indirectly cause the decline of the island fox

Introduced species can compete with, prey upon or transmit disease to native forms, resulting in devastation of indigenous communities. A more subtle but equally severe effect of exotic species is as a supplemental food source for predators that allows them to increase in abundance and then overexploit native prey species. Here we show that the introduction of feral pigs (Sus scrofa) to the California Channel Islands has sustained an unnaturally large breeding population of golden eagles (Aquila chrysaetos), a native predator. The resulting increase in predation on the island fox (Urocyon littoralis) has caused the near extirpation of three subspecies of this endemic carnivore. Foxes evolved on the islands over the past 20,000 years, pigs were introduced in the 1850s and golden eagles, historically, were only transient visitors. Although these three species have been sympatric for the past 150 years, this predator‐prey interaction is a recent phenomenon, occurring within the last decade. We hypothesize that this interaction ultimately stems from human-induced perturbations to the island, mainland and surrounding marine environments.

The behavioural ecology of the island fox (Urocyon littoralis)

Insular populations typically occur at higher densities, have higher survivorship, reduced fecundity, decreased dispersal, and reduced aggression compared to their mainland counterparts. Insularity may also affect mating system and genetic population structure. However, these factors have not been examined simultaneously in any island vertebrate. Here we report on the ecological, behavioural and genetic characteristics of a small carnivore, the island fox Urocyon littoralis, from Fraser Point, Santa Cruz Island, California. Dispersal distances in island foxes are very low (mean 1.39 km, sd 1.26, range 0.16‐3.58 km, n = 8). Home-range size is one of the smallest (mean annual home range = 0.55 km 2 , sd 0.2, n =14) and density is nearly the highest recorded for any canid species (2.4‐15.9 foxes/km 2 ). Similar to other fox species, island foxes are distributed as mated pairs that maintain discrete territories. Overlap among mated pairs was always high (mean 0.85, sd 0.05), while overlap among neighbours (mean 0.11, sd 0.13), regardless of sex, was low. Despite this high degree of territoriality, island foxes are not strictly monogamous. Four of 16 offspring whose parents were identified by paternity analysis were a result of extra-pair fertilizations. Mated pairs were unrelated, however, suggesting inbreeding avoidance. Substantial population differentiation was found between the Fraser Point subpopulation and one only 13 km away (Fst = 0.11). We suggest that the primary effect of finite island area is to limit dispersal, which then influences the demography, behaviour and genetic structure of island fox populations.

DECLINE OF AN ISLAND FOX SUBSPECIES TO NEAR EXTINCTION

Abstract We documented a catastrophic decline in the island fox (Urocyon littoralis littoralis) population on San Miguel Island from 1994 to 1999, and used radiotelemetry to investigate mortality causes in the latter part of the decline. Annual population monitoring via capture-mark-recapture techniques revealed that densities of adult foxes declined up to 100% on 3 trapping grids monitored during the study period. The estimated population size on San Miguel declined from 450 adults in 1994 to less than 20 in 1999. Apparent survival of all age classes declined over the study. A radiotelemetry-based survival study conducted in 1998 and 1999 revealed high winter mortality, most likely due to golden eagle (Aquila chrysaetos) predation. Necropsy of 7 carcasses during the study period confirmed raptor predation for 5 carcasses. Three carcasses were infested with a pathogenic parasite, Angiocaulus gubernaculatus, not found in island fox populations on San Nicolas, San Clemente, Santa Catalina, Santa Cruz, or Santa Rosa Islands, and 2 carcasses had Uncinaria stenocephala and colonic granulomas from Spirocerca infection. Because pup production was low and reproductive effort limited in young females, the island fox population on San Miguel is unlikely to recover without significant intervention. In 1999, 14 island foxes were brought into captivity, and only 1 was known to exist in the wild on San Miguel Island. Resumen Documentamos una declinación catastrófica en la población del zorro Urocyon littoralis littoralis en la Isla de San Miguel entre 1994 y 1999, y usamos radiotelemetría para investigar las causas de la mortalidad en la ultima parte de la declinación. El muestreo anual de la población por medio de técnicas captura-recaptura indicó que la densidad de los zorros adultos declinó hasta un 100% en tres cuadrantes durante el periodo de estudio. El tamaño poblacional estimado en San Miguel declinó de 450 adultos en 1994 a menos de 20 en 1999. La supervivencia aparente de todas clases de edad declinó durante este periodo. Un estudio de supervivencia conducido en 1998 y 1999 por medio de radiotelemetría reveló alta mortalidad durante el invierno, debida probablemente a la depredación por la águila real (Aquila chrysaetos). Análisis postmortem de 7 carcasas durante el estudio confirmó la depredación por aves de presa en 5 carcasas. Tres carcasas fueron infestadas con un parásito patogénico, Angiocaulus gubernaculatus, que no se encuentra en las poblaciones de zorros en las islas de San Nicolás, San Clemente, Santa Catalina, Santa Cruz o Santa Rosa, y 2 carcasas tuvieron Uncinaria stenocephala y granulomas en el colon de la infección Spirocerca. Porque la producción de cachorros fue baja y la capacidad reproductiva limitada en las zorras jóvenes, la población del zorro en San Miguel probablemente no se recupere sin intervención importante. En 1999, 14 zorros fueron apresados para cautiverio, y se sabe de 1 solo zorro que seguía viviendo libre en la isla de San Miguel.

Incorporating Ecological Drivers and Uncertainty into a Demographic Population Viability Analysis for the Island Fox

Biometricians have made great strides in the generation of reliable estimates of demographic rates and their uncertainties from imperfect field data, but these estimates are rarely used to produce detailed predictions of the dynamics or future viability of at-risk populations. Conversely, population viability analysis (PVA) modelers have increased the sophistication and complexity of their approaches, but most do not adequately address parameter and model uncertainties in viability assessments or include important ecological drivers. Merging the advances in these two fields could enable more defensible predictions of extinction risk and better evaluations of management options, but only if clear and interpretable PVA results can be distilled from these complex analyses and outputs. Here, we provide guidance on how to successfully conduct such a combined analysis, using the example of the endangered island fox (Urocyon littoralis), endemic to the Channel Islands of California, USA. This more rigorous demographic PVA was built by forming a close marriage between the statistical models used to estimate parameters from raw data and the details of the subsequent PVA simulation models. In particular, the use of mark-recapture analyses and other likelihood and information-theoretic methods allowed us to carefully incorporate parameter and model uncertainty, the effects of ecological drivers, density dependence, and other complexities into our PVA. Island fox populations show effects of density dependence, predation, and El Nino events, as well as substantial unexplained temporal variation in survival rates. Accounting not only for these sources of variability, but also for uncertainty in the models and parameters used to estimate their strengths, proved important in assessing fox viability with different starting population sizes and predation levels. While incorporating ecological drivers into PVA assessments can help to predict realistic dynamics, we also show that unexplained process variance has important effects even in our extremely well-studied system, and therefore must not be ignored in PVAs. Overall, the treatment of causal factors and uncertainties in parameter values and model structures need not result in unwieldy models or highly complex predictions, and we emphasize that future PVAs can and should include these effects when suitable data are available to support their analysis.

Models of Regional Habitat Quality and Connectivity for Pumas (Puma concolor) in the Southwestern United States

The impact of landscape changes on the quality and connectivity of habitats for multiple wildlife species is of global conservation concern. In the southwestern United States, pumas (Puma concolor) are a well distributed and wide-ranging large carnivore that are sensitive to loss of habitat and to the disruption of pathways that connect their populations. We used an expert-based approach to define and derive variables hypothesized to influence the quality, location, and permeability of habitat for pumas within an area encompassing the entire states of Arizona and New Mexico. Survey results indicated that the presence of woodland and forest cover types, rugged terrain, and canyon bottom and ridgeline topography were expected to be important predictors of both high quality habitat and heightened permeability. As road density, distance to water, or human population density increased, the quality and permeability of habitats were predicted to decline. Using these results, we identified 67 high quality patches across the study area, and applied concepts from electronic circuit theory to estimate regional patterns of connectivity among these patches. Maps of current flow among individual pairs of patches highlighted possible pinch points along two major interstate highways. Current flow summed across all pairs of patches highlighted areas important for keeping the entire network connected, regardless of patch size. Cumulative current flow was highest in Arizona north of the Colorado River and around Grand Canyon National Park, and in the Sky Islands region owing to the many small habitat patches present. Our outputs present a first approximation of habitat quality and connectivity for dispersing pumas in the southwestern United States. Map results can be used to help target finer-scaled analyses in support of planning efforts concerned with the maintenance of puma metapopulation structure, as well as the protection of landscape features that facilitate the dispersal process.

COUPLING STABLE ISOTOPES WITH BIOENERGETICS TO ESTIMATE INTERSPECIFIC INTERACTIONS

Interspecific interactions are often difficult to elucidate, particularly with large vertebrates at large spatial scales. Here, we describe a methodology for estimating interspecific interactions by combining stable isotopes with bioenergetics. We illustrate this approach by modeling the population dynamics and species interactions of a suite of vertebrates on Santa Cruz Island, California, USA: two endemic carnivores (the island fox and island spotted skunk), an exotic herbivore (the feral pig), and their shared predator, the Golden Eagle. Sensitivity analyses suggest that our parameter estimates are robust, and natural history observations suggest that our overall approach captures the species interactions in this vertebrate community. Nonetheless, several factors provide challenges to using isotopes to infer species interactions. Knowledge regarding species-specific isotopic fractionation and diet breadth is often lacking, necessitating detailed laboratory studies and natural history information. However, when coupled with other approaches, including bioenergetics, mechanistic models, and natural history, stable isotopes can be powerful tools in illuminating interspecific interactions and community dynamics.

Does the Order of Invasive Species Removal Matter? The Case of the Eagle and the Pig

Background Invasive species are recognized as a primary driver of native species endangerment and their removal is often a key component of a conservation strategy. Removing invasive species is not always a straightforward task, however, especially when they interact with other species in complex ways to negatively influence native species. Because unintended consequences may arise if all invasive species cannot be removed simultaneously, the order of their removal is of paramount importance to ecological restoration. In the mid-1990s, three subspecies of the island fox Urocyon littoralis were driven to near extinction on the northern California Channel Islands owing to heightened predation by golden eagles Aquila chrysaetos. Eagles were lured to the islands by an abundant supply of feral pigs Sus scrofa and through the process of apparent competition pigs indirectly facilitated the decline in foxes. As a consequence, both pigs and eagles had to be removed to recover the critically endangered fox. Complete removal of pigs was problematic: removing pigs first could force eagles to concentrate on the remaining foxes, increasing their probability of extinction. Removing eagles first was difficult: eagles are not easily captured and lethal removal was politically distasteful. Methodology/Principal Findings Using prey remains collected from eagle nests both before and after the eradication of pigs, we show that one pair of eagles that eluded capture did indeed focus more on foxes. These results support the premise that if the threat of eagle predation had not been mitigated prior to pig removal, fox extinction would have been a more likely outcome. Conclusions/Significance If complete eradication of all interacting invasive species is not possible, the order in which they are removed requires careful consideration. If overlooked, unexpected consequences may result that could impede restoration.