Resource utilization by two insular endemic mammalian carnivores,the island fox and island spotted skunk

We compared resource utilization of two insular endemic mammalian carnivores, the island spotted skunk and island fox, along niche dimensions of space, food, and time on Santa Cruz Island. We predicted that resource use by foxes and skunks would differ along one or more niche dimensions, and that both species would have broader niches or higher densities compared with mainland relatives. Island foxes and island spotted skunks differed to some extent in habitat use, diets, and circadian activity, which may account for their long-term coexistence. Nonetheless, substantial overlap between skunks and foxes in spatial, dietary, and temporal dimensions suggests that competition between the two species does occur. Moreover, competition may be asymmetric, affecting skunks more than foxes. Compared with mainland foxes, island foxes have smaller body size, smaller home range, increased population density, increased diurnal activity, and behavior that is more highly inquisitive and less flightprone all common features of insular faunas. Island skunks, however, apparently have not developed these changes, perhaps due to asymmetric competition with foxes in conjunction with severe ecosystem disturbances caused by feral sheep.     

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-na?ve 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.     

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.     

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.     

Factors Affecting Glucocorticoid and Thyroid Hormone Production of Island Foxes

The island fox (Urocyon littoralis) is native to 6 of the 8 Channel Islands of California, USA. The species experienced a population decline in the 1990s but recovered after predatory golden eagles (Aquila chrysaetos) were relocated and feral pigs (Sus scrofa), a main food source for the eagles, were removed. As part of an ongoing conservation program, the National Park Service conducts yearly health surveys on foxes residing on Santa Rosa and San Miguel islands. In this study, we document non-invasive measures of stress and nutritional status from fecal samples collected during surveys from 2009 to 2015. We collected samples defecated in traps overnight or during handling and measured concentrations of glucocorticoid (GC) and triiodothyronine (T3) metabolites using validated assays. We used generalized linear mixed models to assess the relationships between hormones, season, island, age class, sex, body condition, reproductive status, and ectoparasite presence. Overall, males had marginally lower fecal T3 concentrations than females. Concentrations of both hormones positively correlated with body condition. Fecal GC production varied seasonally; concentrations were highest from December to February and declined through the summer and fall. During summer, younger females and those with signs of recent reproduction had higher fecal GC concentrations than older females or those without evidence of reproduction. Fecal T3 concentrations did not vary in relation to season, age, or reproductive status, but on San Miguel Island were positively correlated with ectoparasite presence. There were no other significant differences between islands. Our results provide hormone data for island foxes and demonstrate that production varies in relation to seasonal and biological factors. These reference data will serve as a comparison for future health surveys and allow managers to identify factors associated with increased stress or reduced nutritional state. © 2019 The Wildlife Society.     

Hematology and serum chemistry of the island fox on Santa Cruz Island

Serum and hematologic biochemistry values for island foxes (Urocyon littoralis) on Santa Cruz Island (California, USA) in April (wet season) and September (dry season) 1998 were evaluated. Serum chemistry of island foxes generally varied seasonally; 10 (40%) of the 25 serum characteristics were higher in the wet season, and three (12%) of the 25 serum characteristics were higher in the dry season. No hematologic parameters varied between seasons, although some measures varied between sexes. Blood analytes also varied with age; fox pups had higher values than adults for one hematologic and four serum parameters, whereas adult foxes had higher values for five hematologic characteristics. The information on blood chemistry provides baseline data useful in the monitoring of this threatened insular endemic carnivore.     

When the Ghost of Predation has Passed: Do Rodents from Islands with and without Fox Predators Exhibit Aversion to Fox Cues?

Anti‐predator behavior can alter the dynamics of prey populations, but little is known about the rate at which anti‐predator behavior is lost from prey populations following predator removal. The Channel Islands differ in whether they have historically contained a top predator, the Island Fox (Urocyon littoralis), in evolutionary time (approximately 6200–10 000 yr). On a historically fox‐containing island and two historically fox‐free islands in 2007, I deployed live traps that contained olfactory cues of fox predators (fox feces), olfactory cues of an herbivore (horse feces) or a no‐feces control. Due to a captive breeding program, foxes on the historically fox‐containing island were effectively removed from 1998 to 2004. Rodents from one of the historically fox‐free islands did not respond to fox cues, whereas rodents on the historically fox‐containing island were more likely to be captured in a control trap and less likely to be captured in a fox‐cue trap. Results from the other historically fox‐free island that experienced a recent population bottleneck and period of captive rearing exhibited a preference for horse‐scented traps. These results suggest that, on islands where foxes are the primary predators, anti‐predator behavior in response to olfactory cues is not likely to be rapidly lost by short‐term removals of foxes, although the nature of anti‐predator behavior may depend upon founder events and recent population dynamics (e.g. population bottlenecks or several generations in captivity).     

Ectoparasites of the island fox on Santa Cruz Island

The ectoparasite fauna for island foxes (Urocyon littoralis) on Santa Cruz Island (California, USA) in April (wet season) and September (dry season) 1998 was evaluated. Three taxa of ectoparasites were identified. These were fleas (Pulex irritans), lice (Neotrichodectes mephitidis), and ticks (Ixodes pacificus). Ectoparasite abundances varied seasonally. Typical of insular endemic species, island foxes may be especially vulnerable to the introduction of novel disease organisms and their vectors.     

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.     

Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis)

Island endemics are typically differentiated from their mainland progenitors in behavior, morphology, and genetics, often resulting from long-term evolutionary change. To examine mechanisms for the origins of island endemism, we present a phylogeographic analysis of whole mitochondrial genomes from the endangered island fox (Urocyon littoralis), endemic to California’s Channel Islands, and mainland gray foxes (U. cinereoargenteus). Previous genetic studies suggested that foxes first appeared on the islands >16,000 years ago, before human arrival (~13,000 cal BP), while archaeological and paleontological data supported a colonization >7000 cal BP. Our results are consistent with initial fox colonization of the northern islands probably by rafting or human introduction ~9200–7100 years ago, followed quickly by human translocation of foxes from the northern to southern Channel Islands. Mitogenomes indicate that island foxes are monophyletic and most closely related to gray foxes from northern California that likely experienced a Holocene climate-induced range shift. Our data document rapid morphological evolution of island foxes (in ~2000 years or less). Despite evidence for bottlenecks, island foxes have generated and maintained multiple mitochondrial haplotypes. This study highlights the intertwined evolutionary history of island foxes and humans, and illustrates a new approach for investigating the evolutionary histories of other island endemics.     

Floreana Island re-colonization potential of the Galápagos short-eared owl (<Emphasis Type="Italic">Asio flammeus galapagoensis</Emphasis>)

Non-native invasive species threaten Galápagos’ endemic biodiversity, and increasing efforts are underway to protect its species from further harm. One such project is focused on the eradication of invasive rodents using rodenticide bait on Floreana, the archipelago’s sixth largest island. Short-eared owls (Asio flammeus galapagoensis) that consume poisoned rodents will, therefore, be at risk of secondary poisoning. If negatively impacted, it is not known to what degree the Floreana Island short-earned owl population is isolated, and whether potential re-colonization exists from its closest neighboring large population on Santa Cruz. Based on eight microsatellite loci and mtDNA control region sequence data from museum and contemporary samples, the short-eared owl populations on Floreana and Santa Cruz are not isolated from each other. However, gene flow is asymmetric from Floreana to Santa Cruz and not in the opposite direction. Morphometric data, including tarsus and bill size, and behavioral observations corroborate the genetic results and suggest that the Floreana population may possess unique traits compared to neighboring populations. For example, Floreana short-eared owls are more crepuscular than neighboring islands, which are predominately nocturnal, and were also non-responsive to inter-island call back recordings. Therefore, these results have important management implications concerning short-eared owl persistence on Floreana following rodenticide application. We recommend that managers implement additional precautions to protect the short-eared owl population until the risk of secondary poisoning has passed such as maintaining individuals in captivity. This study provides no evidence to suggest that short-eared owls are likely to disperse from Floreana’s closest large population on Santa Cruz if the local population is negatively impacted by rodenticide exposure, and the observed morphological and behavioral traits argue against translocating owls between islands.     

Genetic analysis of the endemic island loggerhead shrike, <Emphasis Type="Italic">Lanius ludovicianus anthonyi</Emphasis>

Based on limited research, the island loggerhead shrike, Lanius ludovicianus anthonyi has been considered a distinct subspecies endemic to the northern California Channel Islands. We used mtDNA control region sequences and microsatellite genotyping to compare loggerhead shrikes from the southern California mainland (L. l. gambeli), San Clemente Island (L. l. mearnsi), and the northern islands (L. l. anthonyi). Habitats on the islands are recovering due to the removal of non-native ungulates on the islands, but may be transitioning to habitats less supportive of loggerhead shrikes, so this evaluation comes at a critical time. We utilized 96 museum specimens that were collected over a century to evaluate both spatial and temporal genetic patterns. Analysis of multilocus microsatellite genotypes indicated that historical specimens of loggerhead shrikes (collected between 1897 and 1986) from the two northern islands of Santa Rosa and Santa Cruz are genetically distinct from adjacent mainland and island shrikes. Birds from Santa Catalina Island showed mixed ancestry and did not cluster with the northern island birds. Historical specimens of L. l. mearnsi from San Clemente Island also showed mixed ancestry. Our study provides evidence that a genetically distinct form of loggerhead shrikes, L. l. anthonyi, occurred on the islands of Santa Rosa and Santa Cruz.     

Zoogeography of Pacific Ocean islands: a comparison of the rotifer faunas of Easter Island and the Galápagos archipelago

During September 1990, an extensive sampling of the freshwaters of Easter Island was conducted. The resulting list of rotifer species, supplemented by taxa present in samples collected during a previous trip to the island, is compared with that of another oceanic island of volcanic origin, namely Santa Cruz, Galápagos archipelago. In spite of less research, Santa Cruz has a richer rotifer fauna which, unlike Easter Island, includes endemic species. Possible causes for the faunal poverty of Easter Island are: large source-to-target distance, small target size, uniformity of the target island's ecosystems and limited age of its aquatic biotopes.     

Exome sequencing of deer mice on two California Channel Islands identifies potential adaptation to strongly contrasting ecological conditions

Understanding the forces that drive genotypic and phenotypic change in wild populations is a central goal of evolutionary biology. We examined exome variation in populations of deer mice from two of the California Channel Islands: Peromyscus maniculatus elusus from Santa Barbara Island and P. m. santacruzae from Santa Cruz Island exhibit significant differences in olfactory predator recognition, activity timing, aggressive behavior, morphology, prevalence of Sin Nombre virus, and population densities. We characterized variation in protein‐coding regions using exome capture and sequencing of 25 mice from Santa Barbara Island and 22 mice from Santa Cruz Island. We identified and examined 386,256 SNPs using three complementary methods (BayeScan, pcadapt, and LFMM). We found strong differences in molecular variation between the two populations and 710 outlier SNPs in protein‐coding genes that were detected by all three methods. We identified 35 candidate genes from this outlier set that were related to differences in phenotypes between island populations. Enrichment analyses demonstrated that patterns of molecular variation were associated with biological processes related to response to chemical stimuli and regulation of immune processes. Candidate genes associated with olfaction (Gfy, Tlr2, Vmn13r2, numerous olfactory receptor genes), circadian activity (Cry1), anxiety (Brca1), immunity (Cd28, Eif2ak4, Il12a, Syne1), aggression (Cyp19a, Lama2), and body size (Bc16, Syne1) exhibited non‐synonymous mutations predicted to have moderate to large effects. Variation in olfaction‐related genes, including a stop codon in the Santa Barbara Island population, suggests loss of predator‐recognition traits at the molecular level, consistent with a lack of behavioral aversion to fox feces. These findings also suggest that divergent pathogen prevalence and population density may have influenced adaptive immunity and behavioral phenotypes, such as reduced aggression. Overall, our study indicates that ecological differences between islands are associated with signatures of selection in protein‐coding genes underlying phenotypes that promote success in those environments.     

Impacts of an invasive ant species on roosting behavior of an island endemic flying‐fox

Introduced species can cause major disruptions to ecosystems, particularly on islands. On Christmas Island, the invasive yellow crazy ant (Anoplolepis gracilipes) has detrimental impacts on many animals ranging from the iconic red crabs (Gecarcoidea natalis) to the Christmas Island Thrush (Turdus poliocephalus erythropleurus). However, the full extent of its effects on the island's fauna is not yet known. In this study, we investigated the impact of the yellow crazy ants on the island's last native mammal: the Christmas Island flying‐fox (Pteropus natalis). This species has been described as a keystone species, but has recently experienced substantial population decline to the extent that it is now listed as Critically Endangered. We examined the impacts of the yellow crazy ants on the roosting behavior of the Christmas Island flying‐fox, and on its local and island‐wide distribution patterns. We showed that the crazy ants increased behaviors in the flying‐foxes that were associated with avoidance of noxious stimuli and decreased behaviors associated with resting. Roost tree selection and roost site location were not related to variation in the abundance of crazy ants on the island. Our results indicate that the crazy ants interfere with the activity budgets of the flying‐foxes. However, the flying‐foxes failed to relocate to ant‐free roost trees or roost sites when confronted with the noxious ant, suggesting that the flying‐foxes are either not sufficiently disturbed to override strong cultural attachment to roosts, or, are behaving maladaptively due to ecological naïveté.     

Measuring Recruitment in an Invasive Species to Determine Eradication Potential

ABSTRACT Optimal management of invasive pests can benefit from quantitative measures of rates of recruitment, and particularly, relative contributions of immigration and reproduction. However, these vital rates are difficult to estimate by trapping or observation. Recent studies have demonstrated that analyses with DNA markers may provide detailed information on the origin of immigrants into pest populations, but these studies have not provided comparable data on reproductive rates. We integrated genetic and demographic information from a unique longitudinal data set to comprehensively quantify recruitment during the past 15 years into an island population of red foxes (Vulpes vulpes) and to reveal relative contributions of immigration and reproduction. This population established 100 years ago and persists despite several decades of management aimed at population suppression. Primary source of recruits on the island was in situ reproduction (>95%/annum), although the number of foxes reproducing was small relative to the total number present. Immigration occurred at rates up to 3.6%/annum and was primarily by dispersing males, but is unlikely to be demographically important. We also show that although fox control effectively reduced fox density, there was evidence that control did not reduce the net number of recruits, most likely because the population exhibited a density-dependent release from reproductive suppression. Our results imply that fox control on Phillip Island should primarily focus on reducing on-island abundance and reproduction, but eradication will not be sustained unless immigration ceases.     

A new species of White‐eye Zosterops and notes on other birds from Vanikoro,Solomon Islands

A new species of white‐eye, the Vanikoro White‐eye Zosterops gibbsi, is described from the island of Vanikoro (= Vanikolo) in the Santa Cruz Islands (= Temotu Province) within the Solomon Islands. It differs from the geographically closest white‐eye, the Santa Cruz White‐eye Zosterops sanctaecrucis, by a number of features including a much longer bill, and different leg‐ and eye‐ring colour. This is the second bird species endemic to Vanikoro; the neighbouring Nendo Island supports three endemic species. Although the conservation status of this species appears to be secure, the Santa Cruz Islands are very poorly known. Despite supporting several globally threatened species, the Islands at present are not protected by any conservation activity.     

Geographical distribution pattern and interisland movements of Orii’s flying fox in Okinawa Islands, the Ryukyu Archipelago, Japan

The study of mobile animals such as flying foxes in insular habitats involves clarifying the population status on each island and determining the factors affecting movement patterns among the islands in their distributional range. We visited 25 of the Okinawa Islands and documented the number of Orii’s flying foxes Pteropus dasymallus inopinatus from August 2005 to May 2006. We also conducted a monthly road census on the main island (Okinawa-jima Island) and six adjacent islands from June 2006 to January 2007 and counted the number of fruit-bearing trees of the bats’ four main food plants. The results of classification and regression tree analysis suggested that distance from the main island was a primary factor in determining the distribution pattern and population size of this flying fox, whereas island area, number of plant species, and food availability did not directly affect population size. The number of flying foxes on each island tended to decrease with an increase in distance from the main island; no flying foxes existed on islands >30 km away from the main island. On the other hand, the results of the monthly census showed that the population size on each island fluctuated seasonally. Individuals may move between islands in response to seasonal changes in food availability. In conclusion, the distribution and abundance of Orii’s flying foxes in the Okinawa Islands may be determined by the rate of immigration/emigration, depending on each island’s distance from the main island. Seasonal changes in food availability may act as a trigger for interisland movement, but that movement may be restricted by island connectivity.     

Recent invasion of European red foxes (Vulpes vulpes) on to Fraser Island (K'gari) and South Stradbroke Island

Invasive predators are globally significant drivers of threatened fauna population decline and extinction, and the early detection of new incursions is critical to the chances of successful predator eradication and fauna conservation. Here, we provide evidence of the recent invasion of European red foxes (Vulpes vulpes) on to two large and internationally significant islands off the southeast coast of Queensland, Australia – Fraser Island (K'gari) and South Stradbroke Island. From camera trap footage collected on Fraser Island since 2009, foxes have now been observed on seven different occasions between 2012 and 2016. Two scats collected on South Stradbroke Island in 2013 and 2014 tested positive for fox DNA (and negative for Canis spp. DNA), with fox presence confirmed by subsequent camera trap footage in 2016. These data confirm the recent incursion of foxes on to these islands and suggest that small populations now exist there. Fraser Island and South Stradbroke Island represent key RAMSAR wetland areas of refuge for populations of multiple threatened fauna that have never been previously been exposed to foxes. Fox impacts on these fauna can only be expected to increase without management intervention to eradicate them before they become widespread.