David K. Garcelon

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.

Pathogen exposure in endangered island fox (Urocyon littoralis) populations: Implications for conservation management

Abstract Island fox (Urocyon littoralis) populations on four California Channel Islands have declined severely since 1994. Canine distemper (CDV) was suspected to be responsible for the decline of the Santa Catalina Island fox, so knowledge of infectious disease exposure in the remaining island fox populations was urgently needed. This study reviewed previous pathogen exposure in island foxes and investigated the current threat by conducting a serologic survey of foxes on all islands and sympatric feral cats on three islands from 2001 to 2003 for antibodies against canid pathogens. Before the decline, foxes had evidence of exposure to CDV, canine adenovirus (CAV), canine parvovirus (CPV), and Toxoplasma, with exposure to these five pathogens differing greatly by island. Exposure to canine coronavirus (CCV), canine herpesvirus (CHV), and Leptospira was rare. In 2001–2003, wild-born foxes had evidence of exposure to CDV (5.2–32.8%) on 5 of 6 islands, CPV (28–100%) and CAV (4.7–100%) on five islands, and Toxoplasma gondii (2.3–15.4%) on four islands. Exposure to CCV, CHV and Leptospira was less common. Sharing of infectious agents between sympatric foxes and feral cats appeared minimal, but CDV exposure was detected in two cats on Santa Catalina Island. Domestic dogs have historically been present on the islands, but it is not known if canine diseases can be maintained in fox populations without the continual presence of dogs. Targeted vaccination programs against the most virulent pathogens and continued intensive disease surveillance may help protect the critically small remaining fox populations from disease outbreaks that could threaten the success of ongoing conservation efforts.

A SUSPECTED CANINE DISTEMPER EPIDEMIC AS THE CAUSE OF A CATASTROPHIC DECLINE IN SANTA CATALINA ISLAND FOXES (UROCYON LITTORALIS CATALINAE)

The island fox (Urocyon littoralis catalinae) population on Santa Catalina Island, California, USA declined precipitously in 1999 with an approximate 95% reduction on their eastern range, an area representing 87% of the island. During this investigation, between October 1999 and April 2000, evidence of live foxes dramatically decreased. The only carcass recovered during the decline succumbed to a co-infection of canine distemper virus (CDV) and toxoplasmosis. Sequence analysis of the viral P gene, derived by polymerase chain reaction, indicated that the virus was closely related to CDV from a mainland USA raccoon (Procyon lotor). Nine of 10 foxes trapped in 1999–2000, on the eastern portion of the island after the decline, had serologic evidence of exposure to CDV, whereas only four of 19 foxes trapped in this region in 1998 had antibodies reactive against CDV. The confirmation of CDV in one deceased fox, evidence of exposure to CDV in east-end foxes in 1999–2000 compared to 1998, and documentation of raccoon introductions to the island, implicates canine distemper as the cause of the population decline.

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.

A SEROLOGIC SURVEY OF THE ISLAND FOX (UROCYON LITTORALIS) ON THE CHANNEL ISLANDS, CALIFORNIA

The island fox is listed as a threatened species in California. A serologic survey of 194 island foxes (Urocyon littoralis) was conducted over the entire range of the species on the Channel Islands (California, USA). Antibody prevalence against canine adenovirus and canine parvovirus reached 97% and 59%, respectively, in some populations sampled. Antibody prevalence of canine herpesvirus, canine coronavirus, leptospirosis and toxoplasmosis were low. Antibodies against canine distemper virus were not detected.

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small Ne (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Ne in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.

Induced changes in island fox (Urocyon littoralis) activity do not mitigate the extinction threat posed by a novel predator

Prey response to novel predators influences the impacts on prey populations of introduced predators, bio-control efforts, and predator range expansion. Predicting the impacts of novel predators on native prey requires an understanding of both predator avoidance strategies and their potential to reduce predation risk. We examine the response of island foxes (Urocyon littoralis) to invasion by golden eagles (Aquila chrysaetos). Foxes reduced daytime activity and increased night time activity relative to eagle-naïve foxes. Individual foxes reverted toward diurnal tendencies following eagle removal efforts. We quantified the potential population impact of reduced diurnality by modeling island fox population dynamics. Our model predicted an annual population decline similar to what was observed following golden eagle invasion and predicted that the observed 11% reduction in daytime activity would not reduce predation risk sufficiently to reduce extinction risk. The limited effect of this behaviorally plastic predator avoidance strategy highlights the importance of linking behavioral change to population dynamics for predicting the impact of novel predators on resident prey populations.

DDE Poisoning in an Adult Bald Eagle

A 12-year-old female bald eagle (Haliaeetus leucocephalus) was found in May 1993 on Santa Catalina Island, California (USA), in a debilitated condition, exhibiting ataxia and tremors; it died within hours. On necropsy, the bird was emaciated but had no evidence of disease or physical injury. Chemical analyses were negative for organophosphorus pesticides and lead poisoning. High concentrations of DDE (wet weight basis) were found in the brain (212 ppm), liver (838 ppm), and serum (53 ppm). Mobilization of DDE, from depleted fat deposits, probably resulted in the lethal concentration in the eagles brain.