Darwin's Fox: A Distinct Endangered Species in a Vanishing Habitat

The temperate rain forest of Chiloé Island, Chile, is inhabited by an endemic fox ( Dusicyon fulvipes ) first described by Charles Darwin and now designated Darwin's fox. Despite morphological differences, Darwin's fox has been considered only an insular subspecies of the mainland chilla fox ( D. griseus ). This follows the assumption that the island population, with an estimated population of less than 500, has been separated from the mainland chilla fox for only about 15,000 years and may have received occasional immigrants from the mainland. Consequently, this island population has not been protected as endangered or bred in captivity. Recently, a population of Darwin's fox was discovered on the Chilean mainland 600 km north of Chiloé Island. This population exists in sympatry with chilla and possibly culpeo ( D. culpaeus ) foxes, which suggests that Darwin's fox may be reproductively isolated. To clarify the phylogenetic position of Darwin's fox, we analyzed 344 bp of mitochondrial DNA control-region sequence of the three species of Chilean foxes. Darwin's foxes from the island and mainland populations compose a monophyletic group distinct from the two other Chilean fox species. This indicates that Darwin's fox was probably an early inhabitant of central Chile, and that its present distribution on the mainland may be a relict of a once much wider distribution. Our results highlight the ability of molecular genetic techniques to uncover historical relationships masked by recent events, such as local extinctions. The "rediscovery" of Darwin's fox as a distinct species implies that greater significance should be given to the protection of this species and its unique habitat and to documenting the extent of its mainland distribution.     

Double Allee Effects and Extinction in the Island Fox

Abstract:  An Allee effect (AE) occurs in populations when individuals suffer a decrease in fitness at low densities. If a fitness component is reduced (component AE), per capita population growth rates may decline as a consequence (demographic AE) and extinction risk is increased. The island fox ( Urocyon littoralis ) is endemic to six of the eight California Channel Islands. Population crashes have coincided with an increase in predation by Golden Eagles ( Aquila chrysaetos ). We propose that AEs could render fox populations more sensitive and may be a likely explanation for their sharp decline. We analyzed demographic data collected between 1988 and 2000 to test whether fox density (1) influences survival and reproductive rates; (2) interacts with eagle presence and affects fox fitness parameters; and (3) influences per capita fox population trends. A double component AE simultaneously influenced survival (of adults and pups) and proportion of breeding adult females. The adult survival AE was driven by predation by eagles. These component AEs led to a demographic AE. Multiple-component AEs, a predation-driven AE, and the simultaneous occurrence of both component and demographic AEs in a mammal are all previously unreported processes. Populations below 7 foxes/km² could have suboptimal population growth rates due to the demographic AE, and AEs may have contributed to the dramatic declines in three fox populations. Because fox densities in critically endangered populations are well below this level, removing Golden Eagles appears necessary to prevent a predation-driven AE. Conservationists should also be aware of AEs when planning the release of captive foxes. More generally, our findings highlight the danger of overlooking AEs in the conservation of populations of rare or threatened species.     

Hybridization in the Island Endemic, Catalina Mahogany

Abstract: Allozyme data, combined with traditional morphological and anatomical data, were used to evaluate the genetic status of the island endemic, Cercocarpus traskiae (Catalina mahogany). Comprising only seven adult plants and close to 70 seedlings, C. traskiae is confined to Wild Boar Gully on the southwest side of Santa Catalina Island in Los Angeles County, California Electrophoretic examination of 22 enzyme loci revealed that all but two of the seven adult C. traskiae trees were unique allozymically. Furthermore four of the seven C. traskiae individuals were morphologically and/or anatomically intermediate between "true" C. traskiae and the more abundant Cercocarpus species on Santa Catalina, C. betuloides var, blancheae . Further electrophoretic analyses revealed that two of these four individuals possessed an additive "hybrid" enzyme phenotype indicating that these individuals were hybrid. Twenty-five of the seedlings were also assayed but none of the seedlings displayed hybrid enzyme phenotypes.
Given the evidence for hybridization described herein, we make two suggestions to enhance the long-term preservation of C. traskiae . First, it may be desirable to eliminate the single C. betuloides var.: blancheae individual in Wild Boar Gully. Second, we suggest that established cuttings of true C. traskiae be transplanted to areas on Santa Catalina where the probability of hybridization is minimal Our data further demonstrate that accurate taxonomic identification and an understanding of population genetic structure are necessary for the enlightened management of small relict populations or island endemics.     

Flying Foxes as Strong Interactors in South Pacific Island Ecosystems: A Conservation Hypothesis

Abstract: The dependency of highly endemic island floras on few potential pollinators in depauperate island faunas suggests that pollinators and seed dispersers may be crucial in the preservation of biodiversity in isolated oceanic islands. We discuss the hypothesis that flying foxes are "strong interactors" in South Pacific islands where they serve as the principal pollinators and seed dispersers, This suggests that the ongoing decline and ultimate extinction of flying fox species on Pacific islands may lead to a cascade of linked plant extinctions. We propose an empirical test of this hypothesis: comparisons of plant reproductive success in Guam, which has virtually lost its flying fox populations, and Samoa, where significant populations remain.     

Phenotypic Effects of Cattle Mitochondrial DNA in American Bison

Hybridization between endangered species and more common species is a significant problem in conservation biology because it may result in extinction or loss of adaptation. The historical reduction in abundance and geographic distribution of the American plains bison (Bison bison bison) and their recovery over the last 125 years is well documented. However, introgression from domestic cattle (Bos taurus) into the few remaining bison populations that existed in the late 1800s has now been identified in many modern bison herds. We examined the phenotypic effect of this ancestry by comparing weight and height of bison with cattle or bison mitochondrial DNA (mtDNA) from Santa Catalina Island, California (U.S.A.), a nutritionally stressful environment for bison, and of a group of age‐matched feedlot bison males in Montana, a nutritionally rich environment. The environmental and nutritional differences between these 2 bison populations were very different and demonstrated the phenotypic effect of domestic cattle mtDNA in bison over a broad range of conditions. For example, the average weight of feedlot males that were 2 years of age was 2.54 times greater than that of males from Santa Catalina Island. In both environments, bison with cattle mtDNA had lower weight compared with bison with bison mtDNA, and on Santa Catalina Island, the height of bison with cattle mtDNA was lower than the height of bison with bison mtDNA. These data support the hypothesis that body size is smaller and height is lower in bison with domestic cattle mtDNA and that genomic integrity is important for the conservation of the American plains bison. Efectos Fenotípicos del ADN Mitocondrial de Ganado en el Bisonte Americano     

Adaptive Units for Conservation: Population Distinction and Historic Extinctions in the Island Scrub-Jay

Abstract:  The Island Scrub-Jay ( Aphelocoma insularis ) is found on Santa Cruz Island, California, and is the only insular bird species in the continental United States. We typed seven microsatellite loci and sequenced a portion of the mitochondrial DNA control region of Island Scrub-Jays and their closest mainland relative, the Western Scrub-Jay ( Aphelocoma californica ), to assess levels of variability and effective population size and to examine the evolutionary relationship between the two species. The estimated female effective population size, N _ef, of the Island Scrub-Jay was 1603 (90% confidence interval: 1481–1738) and was about 7.5% of the size of the mainland species. Island and Western Scrub-Jays have highly divergent control-region sequences, and the value of 3.14 ± 0.09% sequence divergence between the two species suggests a divergence time of approximately 151,000 years ago. Because the four northern Channel Islands were joined as one large island as recently as 11,000 years ago, extinctions must have occurred on the three other northern Channel islands, Santa Rosa, San Miguel, and Anacapa, highlighting the vulnerability of the remaining population. We assessed the evolutionary significance of four island endemics, including the Island Scrub-Jay, based on both genetic and adaptive divergence. Our results show that the Island Scrub-Jay is a distinct species of high conservation value whose history and adaptive potential is not well predicted by study of other island vertebrates.     

Critically evaluating best management practices for preventing freshwater turtle extinctions

Ex situ conservation tools, such as captive breeding for reintroduction, are considered a last resort to recover threatened or endangered species, but they may also help reduce anthropogenic threats where it is difficult or impossible to address them directly. Headstarting, or captive rearing of eggs or neonate animals for subsequent release into the wild, is controversial because it treats only a symptom of a larger conservation problem; however, it may provide a mechanism to address multiple threats, particularly near population centers. We conducted a population viability analysis of Australia's most widespread freshwater turtle, Chelodina longicollis, to determine the effect of adult roadkill (death by collision with motor vehicles), which is increasing, and reduced recruitment through nest predation from introduced European red foxes (Vulpes vulpes). We also modeled management scenarios to test the effectiveness of headstarting, fox management, and measures to reduce mortality on roads. Only scenarios with headstarting from source populations eliminated all risks of extinction and allowed population growth. Small increases in adult mortality (2%) had the greatest effect on population growth and extinction risk. Where threats simultaneously affected other life‐history stages (e.g., recruitment), eliminating harvest pressures on adult females alone did not eliminate the risk of population extinction. In our models, one source population could supply enough hatchlings annually to supplement 25 other similar‐sized populations such that extinction was avoided. Based on our results, we believe headstarting should be a primary tool for managing freshwater turtles for which threats affect multiple life‐history stages. We advocate the creation of source populations for managing freshwater turtles that are greatly threatened at multiple life‐history stages, such as depredation of eggs by invasive species and adult mortality via roadkill.     

The Potential for Conservation of Polynesian Birds through Habitat Mapping and Species Translocation

Abstract: The dependency of highly endemic island floras on few potential pollinators in depauperate island faunas suggests that pollinators and seed dispersers may be crucial in the preservation of biodiversity in isolated oceanic islands. We discuss the hypothesis that flying foxes are "strong interactors" in South Pacific islands where they setwe as the principal pollinators and seed dispersers, This suggests that the ongoing decline and ultimate extinction of flying fox species on Pacific islands may lead to a cascade of linked plant extinctions. We propose an empirical test of this hypothesis: comparisons of plant reproductive success in Guam, which has virtually lost its flying fox populations, and Samoa, where signifcant populations remain.     

Flying Foxes (Chiroptera: Pteropodidae): Threatened Animals of Key Ecological and Economic Importance

Abstract: Flying foxes are animals of extraordinary ecological and economic importance throughout forests of the Old World tropics Nearly 200 species play an essential role as forest pollinators and seed dispersers, yet they are frequently misunderstood intensely persecuted and exceptionally vulnerable to extinction Their role in the propagation of numerous important plants remains virtually uninvestigated. However, our review of already available literature demonstrates that at least 289 plant species rely to vatying degrees on large populations of flying foxes for propagation. These plants, in addition to their many ecological contributing produce some 448 economically valuable products. The fact that flying foxes are increasingly threaten and that few baseline data exist on population trends is cause for concern Many appear to be in severe decline, and several species are already extinct. We present initial observations on flying fox importance and survival threats in hopes of highlighting research and conservation needs.     

Avian Survival Rates and the Extinction Process on Barro Colorado Island, Panama

Abstract: Selective extinction following isolation of habitat patches may be due to biogeographical (e.g., island size or isolation) and ecological (species natural histories, interspecifc interactions) factors, or their interactions. Among the demographic and life history attributes commonly associated with high extinction probability are small populations, large size of individuals, and population variability. Long-term capture-recapture data from forest habitat in central Panama permit an examination of the association between mainland survival rates and extinction on a nearby land-bridge island Species of birds that no longer occur on Barro Colorado Island (BCI), Panama, have, on average, lower survival rates on the adjacent mainland than species that have persisted on BCI. Moreover, of the species that no longer occur on BCI, those with lower mainland survival rates generally disappeared earlier from the island. My analysis provides little evidence of a relationship between extinction and population size. Recolonization of BCI from the adjacent mainland by the forest undergrowth species studied here is unlikely. Reduced reproductive success on BCI combined with naturally low adult survival rates seems to be responsible for these BCI extinctions. High nest predation and/or altered landscape dynamics are probable agents in the low reproductive success. The methods used here could be employed in other circumstances to identify fragmentation-sensitive species.     

A link between biologically imported particulate organic nutrients and the detritus food web in reef communities

Previous work with planktivorous fishes has shown that they import particulate organic and inorganic material to reefs in the form of fecal pellets, which, in part, are deposited in crevices on the reef where these fishes shelter during their inactive period. Since these feces do not accumulate in fish shelters, we predicted that some of the feces could be rapidly consumed by reef detritivores. We examined the attractiveness of fish feces to potential reef detritivores by placing traps baited with planktivorous fish feces, along with unbaited control traps, in crevices on rocky reefs at Santa Catalina Island, California, USA, between June 1982 and November 1983, and on coral reefs at St. Croix, U.S. Virgin Islands, during June 1983. Significantly more animals (the majority being crustaceans) were trapped in the baited traps compared to the unbaited controls on both reefs. There was also a significant association between the presence of trapped animals and fish feces at Santa Catalina Island (p = 0.009); this association was not quite as strong in St. Croix (p = 0.069). The consumption by shrimp of feces marked with carmine particles and, in turn, the predation on these shrimp by a reef fish demonstrates the links between this type of imported particulate organic and inorganic material and the food web of the reef community.Please address all correspondence and requests for reprints to Dr. Miller at California State University, Long Beach     

Genetic Analysis of the Endangered Island Endemic Malacothamnus fasciculatus (Nutt.) Greene var. nesioticus (Rob.) Kearn. (Malvaceae)

Isozyme, randomly amplified polymorphic DNA, and ribosomal DNA analyses were used to evaluate the genetic distinctness and diversity of the endangered island endemic Malacothamnus fasciculatus var. nesioticus (Santa Cruz Island bush mallow). Analysis of amplified DNA profiles and electrophoretic data indicates that var. nesioticus is genetically distinct from other varieties within the species. No isozyme or amplified DNA variation was detected among individuals of nesioticus populations, but restriction site analysis of ribosomal DNA revealed the presence of three closely related genotypes within one of the nesioticus populations. Apparent clonal structuring was found in both nesioticus populations and in one mainland population, var. nuttallli . Results from these analyses provide the background necessary for the design of conservation efforts with recovery goals that insure the long-term survival of Malacothamnus fasciculatus var. nesioticus .     

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.     

Biological parameters used in setting captive‐breeding quotas for Indonesia's breeding facilities

The commercial captive breeding of wildlife is often seen as a potential conservation tool to relieve pressure on wild populations, but laundering of wild‐sourced specimens as captive bred can seriously undermine conservation efforts and provide a false sense of sustainability. Indonesia is at the center of such controversy; therefore, we examined Indonesia's captive‐breeding production plan (CBPP) for 2016. We compared the biological parameters used in the CBPP with parameters in the literature and with parameters suggested by experts on each species and identified shortcomings of the CBPP. Production quotas for 99 out of 129 species were based on inaccurate or unrealistic biological parameters and production quotas deviated more than 10% from what parameters in the literature allow for. For 38 species, the quota exceeded the number of animals that can be bred based on the biological parameters (range 100–540%) calculated with equations in the CBPP. We calculated a lower reproductive output for 88 species based on published biological parameters compared with the parameters used in the CBPP. The equations used in the production plan did not appear to account for other factors (e.g., different survival rate for juveniles compared to adult animals) involved in breeding the proposed large numbers of specimens. We recommend the CBPP be adjusted so that realistic published biological parameters are applied and captive‐breeding quotas are not allocated to species if their captive breeding is unlikely to be successful or no breeding stock is available. The shortcomings in the current CBPP create loopholes that mean mammals, reptiles, and amphibians from Indonesia declared captive bred may have been sourced from the wild.     

Unprecedented Low Levels of Genetic Variation and Inbreeding Depression in an Island Population of the Black-Footed Rock-Wallaby

Abstract: It has been argued that demographic and environmental factors will cause small, isolated populations to become extinct before genetic factors have a significant negative impact. Islands provide an ideal opportunity to test this hypothesis because they often support small, isolated populations that are highly vulnerable to extinction. To assess the potential negative impact of isolation and small population size, we compared levels of genetic variation and fitness in island and mainland populations of the black-footed rock-wallaby ( Petrogale lateralis [Marsupialia: Macropodidae]). Our results indicate that the Barrow Island population of P. lateralis has unprecedented low levels of genetic variation (  H _e = 0.053, from 10 microsatellite loci) and suffers from inbreeding depression (reduced female fecundity, skewed sex ratio, increased levels of fluctuating asymmetry). Despite a long period of isolation ( ∼ 1600 generations) and small effective population size (  N _e ∼ 15), demographic and environmental factors have not yet driven this population to extinction. Nevertheless, it has been affected significantly by genetic factors. It has lost most of its genetic variation and become highly inbred (  F _e = 0.91), and it exhibits reduced fitness. Because several other island populations of P. lateralis also exhibit exceptionally low levels of genetic variation, this phenomenon may be widespread. Inbreeding in these populations is at a level associated with high rates of extinction in populations of domestic and laboratory species. Genetic factors cannot then be excluded as contributing to the extinction proneness of small, isolated populations.     

Evaluating the Effectiveness of Predator Control: the Non-Native Red Fox as a Case Study

Abstract: Non-native vertebrate predators pose a severe threat to many native species, and a variety of management programs are aimed at reducing predator effects. We sought to assess the effects of predator-control programs by analyzing changes in prey and predator populations based on data commonly collected in these programs. We examined data from a predator-control program that primarily targets the introduced red fox (  Vulpes vulpes regalis ) in central California. Red foxes negatively affect populations of native waterbirds, particularly the endangered California Clapper Rail (  Rallus longirostris obsoletus ). Using a combination of matrix population modeling, simple difference equations, and statistical analysis, we analyzed data on removed predators and monitored prey populations. Past control efforts succeeded in depressing fox numbers in local areas over 3-month intervals, and there was a significant, positive relationship between the growth rate of local Clapper Rail populations and the successful trapping of red foxes in the preceding year. By modeling the effect of different fox-removal rates, we found that a stable or declining population could be achieved by removing a minimum of 50% of the adults and 25% of the juveniles. Under trapping rates of 50–70%, the proportion of the fox population composed of immigrants averaged 20–52%. In contrast to the current management approach, elasticity analyses suggested that changes in adult survival rates had relatively little effect on long-term population growth. Overall, our approach indicated that predator control was effective in the short term, but for longer-term success it may be necessary to redirect efforts to control juvenile and immigrant foxes. Our analytical approach is potentially useful for evaluating current control programs aimed at reducing the effects of predators on native species.     

Isolation and population divergence of a widespread Indo-West Pacific marine gastropod at Easter Island

Oceanic islands represent excellent systems for studying the link between geographic isolation and population divergence. Easter Island is the world’s most isolated island and exhibits a high level of endemicity in the nearshore marine environment. Yet few studies have examined the effect of such extreme isolation on the divergence of populations of widespread species that occur at Easter Island. Conus miliaris, a marine gastropod distributed throughout much of the Indo-West Pacific, occurs at Easter Island where the population is ecologically and morphologically distinct from other populations of the species. To determine whether these phenotypic differences are associated with genetic isolation of the Easter Island population, we investigated the phylogeography of this species by examining mitochondrial COI sequences obtained from 141 individuals from eight localities occurring predominantly in the western, central and southeastern Pacific. Results from our analyses show that C. miliaris at Easter Island differs genetically from other populations. We estimate that C. miliaris colonized Easter Island shortly after the origin of the island ≤0.7 million years ago and that since population founding, gene flow has occurred predominantly from Easter Island to the west and that little migration has occurred into Easter Island.     

Flying foxes cease to function as seed dispersers long before they become rare

Rare species play limited ecological roles, but particular behavioral traits may predispose species to become functionally extinct before becoming rare. Flying foxes (Pteropodid fruit bats) are important dispersers of large seeds, but their effectiveness is hypothesized to depend on high population density that induces aggressive interactions. In a Pacific archipelago, we quantified the proportion of seeds that flying foxes dispersed beyond the fruiting canopy, across a range of sites that differed in flying fox abundance. We found the relationship between ecological function (seed dispersal) and flying fox abundance was nonlinear and consistent with the hypothesis. For most trees in sites below a threshold abundance of flying foxes, flying foxes dispersed < 1% of the seeds they handled. Above the threshold, dispersal away from trees increased to 58% as animal abundance approximately doubled. Hence, flying foxes may cease to be effective seed dispersers long before becoming rare. As many species' populations decline worldwide, identifying those with threshold relationships is an important precursor to preservation of ecologically effective densities.     

Regional extinction of a conspicuous dorid nudibranch (Mollusca: Gastropoda) in California

Felimare californiensis (=Hypselodoris californiensis) was once common throughout the Southern California Bight (SCB) and California Channel Islands. This well-known shallow-water nudibranch, which specializes on dysideid sponges, has persisted for decades in Mexico, but in California disappeared from its entire range by 1984. Since reappearing in 2003, it has been found only at Santa Catalina Island, plus sightings of single individuals in 2011 at Santa Cruz Island and San Diego. The decline of F. californiensis in California was documented using published historical records, museum collections, unpublished field accounts, and images posted online. The loss of this emblematic species is unique among Californian nudibranchs, including (1) its congener Felimare porterae (=Mexichromis porterae), with which it appears to overlap in diet, and (2) opisthobranch species with similar historical geographic ranges and mode of development. The decline in F. californiensis is not predicted by warming trends and climate variation over the past 40 years, including the strong El Niño events of 1983 and 1998. Coastal pollution from the large human population in southern California may have impacted Dysidea amblia, the primary reported prey of F. californiensis. Historical overcollecting of the nudibranch and habitat loss through the development of major ports likely also contributed to its decline. Sightings since 2003 are consistent with a nascent recovery, as elements of water quality have improved in the SCB in recent decades.