Timothy J. Coonan

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.

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.

SPATIAL AND TEMPORAL VARIATION IN THE SEROPREVALENCE OF CANINE HEARTWORM ANTIGEN IN THE ISLAND FOX

Island foxes (Urocyon littoralis) are endemic to six of the eight California Channel Islands (USA). The island fox is classified as a threatened species by the State of California, and recently three of the six subspecies have experienced abrupt population declines. As part of a continuing effort to determine the cause of the declines, we tested island fox serum samples collected in 1988 (n = 176) and 1997–98 (n = 156) over the entire geographic range of the species for seroprevalence of canine heartworm (Dirofilaria immitis) antigen. Using a commercially available enzyme-linked immunosorbent assay (PetChek®, Idexx Laboratories, Westbrook, Maine, USA) we detected heartworm antigen in four of the six populations of island foxes. On San Miguel and Santa Rosa Islands, seroprevalence in adult foxes was >85% (n = 62) in 1988 and increased to 100% (n = 24) in 1997–98. On Santa Cruz Island, seroprevalence in adult foxes decreased from 83% (n = 30) to 58% (n = 26), whereas on San Nicolas Island, seroprevalence increased from 25% (n = 32) to 77% (n = 30) during the same period. All of the pups assayed (n = 33) were seronegative. The seroprevalences of heartworm reported herein for the four populations of island foxes are the highest yet reported for a fox species. However, additional demographic data reported elsewhere suggests that heartworm has not been a major factor in the recent declines of island fox populations.

Angiocaulus gubernaculatus in the Island Fox (Urocyon littoralis) From the California Channel Islands and Comments on the Diagnosis of Angiostrongylidae Nematodes in Canid and Mustelid Hosts

Adult nematode parasites were recovered from the heart blood of a deceased island fox (Urocyon littoralis) submitted for necropsy to determine the cause of death. Examination of the recovered nematodes supported the generic diagnosis of Angiocaulus, a parasite in Angiostrongylidae found in domestic and wild canids and mustelids. Specific diagnosis of the worms from the island fox as Angiocaulus gubernaculatus is based on the morphology of the dorsal ray in the copulatory bursa of the male worm and its comparison with published descriptions of Angiocaulus raillieti and A. gubernaculatus. Although A. gubernaculatus has been typically associated with mustelid hosts, its occurrence in the island fox indicates that the host distribution for the parasite may not be as restricted as previously believed.

BIOCHEMICAL AND HEMATOLOGIC REFERENCE INTERVALS FOR THE ENDANGERED ISLAND FOX (UROCYON LITTORALIS)

Hematologic and serum biochemical data collected must be interpreted by comparison with normal reference intervals generated from healthy animals, within a similar population, because many blood parameters are influenced by diet, environment, and stress. Species-specific reference intervals for the endangered island fox (Urocyon littoralis) are not available. We reviewed hematology and serum biochemistry panels from 280 island foxes sampled from 1999–2008 and established normal reference intervals from clinically healthy foxes using a nonparametric approach. Blood parameters were analyzed for differences in age, sex, island of origin, and captivity status. Alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase, and creatine kinase activities, as well as calcium and phosphorus concentrations, were significantly higher in juveniles than in adults, but total protein and globulin concentration was lower for juveniles than for adults. Lymphocyte and eosinophil counts, and blood urea nitrogen (BUN) concentration, in foxes from the northern Channel islands of California, USA (Santa Cruz, Santa Rosa, and San Miguel) were higher when compared with foxes from Santa Catalina Island to the south. Higher lymphocyte and eosinophil numbers in the northern island foxes may be associated with increased levels of parasitism on the northern islands. Differences in BUN concentration in both free-ranging and captive foxes may reflect dietary differences among islands. Although aggressive conservation programs have been enacted, island foxes are still susceptible to infectious and neoplastic diseases and, potentially, to toxins. Island fox species-specific reference intervals will enable managers and veterinarians to better care for sick and injured foxes and will contribute to future population health monitoring.

Ghost prey and missing conflicts: reinterpreting the implications of bald eagle diet composition on the California Channel Islands.

The study by Newsome et al. (1) presented an approach to evaluating the historic ecological role of bald eagles (Haliaeetus leucocephalus) on the California Channel Islands (CI). Unfortunately, they ignore an alternative explanation for some of their data and overinterpret their results, leading to conclusions that are not the most parsimonious (1).

Home-range size and habitat selection by male Island Foxes (Urocyon littoralis) in a Low-Density Population

Abstract Island foxes (Urocyon littoralis) are listed as federally endangered on four of the six California Channel Islands to which they are endemic. The population on Santa Rosa Island declined by 99% during the 1990s due to golden eagle (Aguila chrysaetos) predation but is now recovering. This drastic population reduction provided an unprecedented opportunity to study home-range size and habitat use at very low levels of intraspecific competition. We used global positioning system (GPS) collars to track 14 adult male foxes from September 2009 through June 2010. On average, the collars operated for 16.5 wk, yielding 364 locations per fox. The 95% minimum convex polygon home ranges averaged 3.39 km2, which is several times larger than reported in previous studies conducted at higher population densities. We used Euclidean distance analysis to assess habitat selection within 95% kernel density isopleth (KDI) home ranges and 50% KDI core areas. The foxes used most of the available vegetation types but exhi...