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.     

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.     

Food webs and intraguild predation: community interactions of a native mesocarnivore

Trophic level interactions between predators create complex relationships such as intraguild predation. Theoretical research has predicted two possible paths to stability in intraguild systems: intermediate predators either outcompete higher-order predators for shared resources or select habitat based on security. The effects of intraguild predation on intermediate mammalian predators such as swift foxes (Vulpes velox) are not well understood. We examined the relationships between swift foxes and both their predators and prey, as well the effect of vegetation structure on swift fox-coyote (Canis latrans) interactions, between August 2001 and August 2004. In a natural experiment created by the Pinon Canyon Maneuver Site in southeastern Colorado, USA, we documented swift fox survival and density in a variety of landscapes and compared these parameters in relation to prey availability, coyote abundance, and vegetation structure. Swift fox density varied significantly between study sites, while survival did not. Coyote abundance was positively related to the basal prey species and vegetation structure, while swift fox density was negatively related to coyote abundance, basal prey species, and vegetation structure. Our results support the prediction that, under intraguild predation in terrestrial systems, top predator distribution matches resource availability (resource match), while intermediate predator distribution inversely matches predation risk (safety match). While predation by coyotes may be the specific cause of swift fox mortality in this system, the more general mechanism appears to be exposure to predation moderated by shrub density.     

Potential Misuse of Avian Density as a Conservation Metric

Abstract: Effective conservation metrics are needed to evaluate the success of management in a rapidly changing world. Reproductive rates and densities of breeding birds (as a surrogate for reproductive rate) have been used to indicate the quality of avian breeding habitat, but the underlying assumptions of these metrics rarely have been examined. When birds are attracted to breeding areas in part by the presence of conspecifics and when breeding in groups influences predation rates, the effectiveness of density and reproductive rate as indicators of habitat quality is reduced. It is beneficial to clearly distinguish between individual‐ and population‐level processes when evaluating habitat quality. We use the term reproductive rate to refer to both levels and further distinguish among levels by using the terms per capita fecundity (number of female offspring per female per year, individual level) and population growth rate (the product of density and per capita fecundity, population level). We predicted how density and reproductive rate interact over time under density‐independent and density‐dependent scenarios, assuming the ideal free distribution model of how birds settle in breeding habitats. We predicted population density of small populations would be correlated positively with both per capita fecundity and population growth rate due to the Allee effect. For populations in the density‐dependent growth phase, we predicted no relation between density and per capita fecundity (because individuals in all patches will equilibrate to the same success rate) and a positive relation between density and population growth rate. Several ecological theories collectively suggest that positive correlations between density and per capita fecundity would be difficult to detect. We constructed a decision tree to guide interpretation of positive, neutral, nonlinear, and negative relations between density and reproductive rates at individual and population levels.     

A population viability analysis for the Island Fox on Santa Catalina Island,California

The island fox (Urocyon littoralis) on Santa Catalina Island is among the most imperiled species on the Channel Islands due to a recent outbreak of canine distemper virus (CDV). The western subpopulation, which was not exposed to CDV, is a crucial element in the recovery of foxes by providing a source of animals for translocation and captive breeding. Using the program VORTEX, we developed a population viability analysis for the Santa Catalina Island fox to (1) address the likelihood of population persistence, (2) estimate the current susceptibility of the population to catastrophic events, and (3) evaluate the efficacy of current restoration strategies of releasing captive bred foxes and transplanting wild animals. Overall, we found the population to be susceptible to catastrophic events; a 50% increase in mortality every 20 years was sufficient to elevate the extinction risk above 5%. Current management activities entail the transplanting of 12 juvenile foxes annually, which may reduce the viability of the western subpopulation. A minimum population size of at least 150 foxes should be maintained in each subpopulation to reduce the risk of extinction due to demographic stochasticity. Releases of translocated and captive bred animals affect the speed of recovery on the eastern half of Catalina Island, but not the probability of extinction, which is near zero under current conditions. We conducted a sensitivity analysis for demographic parameters by incrementally varying survival, fecundity and density-dependence parameters, while holding all other parameters constant. Sensitivity analyses identified mortality and mean litter size as the most sensitive parameters, while the implementation of density-dependence and environmental variation of model parameters did not seem to affect population performance. We conclude that the population of island foxes on Santa Catalina is currently at a critically low population level, but recovery of the species appears possible.     

Fitness costs of dispersal in red foxes (Vulpes vulpes)

The costs of dispersal are an important factor promoting natal philopatry, thereby encouraging the formation of social groups. The red fox, Vulpes vulpes, exhibits a highly flexible social system and one that is thought to represent a possible stage in the evolution of more complex patterns of group-living. Although the potential benefits accruing to philopatric offspring have previously been studied in this species, the potential costs of dispersal have received less attention. We contrasted survival rates, nutritional status, injuries and reproductive output of dispersing and non-dispersing male and female foxes in an urban population to assess the relative costs of dispersal versus natal philopatry. Mortality rates were not significantly higher for dispersing foxes, either in the short- or long-term. There was no evidence of increased nutritional stress in dispersing individuals. Dispersing individuals did, however, exhibit greater levels of wounding, although this did not appear to affect survival. Dispersing females were more likely to miss a breeding opportunity early in their reproductive lifespan. In contrast, both dispersing and non-dispersing males were unlikely to breed in their first year. We conclude that the major fitness component in females affected by dispersing is age at first reproduction.     

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.     

Bald eagles and sea otters in the Aleutian Archipelago: indirect effects of trophic cascades

Because sea otters (Enhydra lutris) exert a wide array of direct and indirect effects on coastal marine ecosystems throughout their geographic range, we investigated the potential influence of sea otters on the ecology of Bald Eagles (Haliaeetus leucocephalus) in the Aleutian Islands, Alaska, USA. We studied the diets, productivity, and density of breeding Bald Eagles on four islands during 1993-1994 and 2000-2002, when sea otters were abundant and scarce, respectively. Bald Eagles depend on nearshore marine communities for most of their prey in this ecosystem, so we predicted that the recent decline in otter populations would have an indirect negative effect on diets and demography of Bald Eagles. Contrary to our predictions, we found no effects on density of breeding pairs on four islands from 1993-1994 to 2000-2002. In contrast, diets and diet diversity of Bald Eagles changed considerably between the two time periods, likely reflecting a change in prey availability resulting from the increase and subsequent decline in sea otter populations. The frequency of sea otter pups, rock greenling (Hexagammus lagocephalus), and smooth lumpsuckers (Aptocyclus ventricosus) in the eagle's diet declined with corresponding increases in Rock Ptarmigan (Lagopus mutus), Glaucous-winged Gulls (Larus glaucescens), Atka mackerel (Pleurogrammus monopterygius), and various species of seabirds during the period of the recent otter population decline. Breeding success and productivity of Bald Eagles also increased during this time period, which may be due to the higher nutritional quality of avian prey consumed in later years. Our results provide further evidence of the wide-ranging indirect effects of sea otter predation on nearshore marine communities and another apex predator, the Bald Eagle. Although the indirect effects of sea otters are widely known, this example is unique because the food-web pathway transcended five species and several trophic levels in linking one apex predator to another.     

Raptors and Red Grouse: Conservation Conflicts and Management Solutions

Abstract: Recovering predator populations may present problems for conservationists if their prey are of economic or conservation value. We address this issue by examining the conflict between raptor conservation and management of Red Grouse (   Lagopus l. scoticus ) in Britain. Heather moorland is a distinctive habitat that supports an important assemblage of breeding birds. Large areas of moorland are managed by private landowners for shooting grouse. Although grouse shooting benefits conservation by retaining heather moorland, it is currently unclear whether grouse management directly benefits other upland birds. Human persecution has greatly restricted the range and abundance of most raptor species in Britain. Following the introduction of bird protection laws, the decline in gamekeeping, and the restriction of organochlorine pesticides, raptor populations have started to recover. Persecution of raptors on grouse moors is widespread and limits the range and abundance of Hen Harriers (  Circus cyaneus ), Peregrine Falcons (   Falco peregrinus ), and Golden Eagles ( Aquila chrysaetos ). In some circumstances, raptor predation can reduce both the breeding density and productivity of Red Grouse. Limitation of grouse populations through raptor predation is most likely to occur where raptors are at high density because of the abundance of alternative prey, and grouse are at low density either because of poor management or the cyclic nature of some grouse populations. In the long term, habitat management may reduce densities of alternative prey, leading to reductions in raptor densities and their predation on grouse. More active intervention may be required, however, if grouse moors are to remain viable in the short-term. Current research is focused on manipulating harrier diet through diversionary feeding. Complementary research is needed to investigate methods to reduce raptor numbers locally while ensuring their national status.     

Decoupling of component and ensemble density feedbacks in birds and mammals

A component density feedback represents the effect of change in population size on single demographic rates, whereas an ensemble density feedback captures that effect on the overall growth rate of a population. Given that a population's growth rate is a synthesis of the interplay of all demographic rates operating in a population, we test the hypothesis that the strength of ensemble density feedback must augment with increasing strength of component density feedback, using long-term censuses of population size, fertility, and survival rates of 109 bird and mammal populations (97 species). We found that compensatory and depensatory component feedbacks were common (each detected in approximately 50% of the demographic rates). However, component feedback strength only explained <10% of the variation in ensemble feedback strength. To explain why, we illustrate the different sources of decoupling between component and ensemble feedbacks. We argue that the management of anthropogenic impacts on populations using component feedbacks alone is ill-advised, just as managing on the basis of ensemble feedbacks without a mechanistic understanding of the contributions made by its components and environmental variability can lead to suboptimal decisions.     

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.     

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.     

Experimental examination of behavioural interactions between free-ranging wild and domestic canids

The structure of mammalian carnivore communities is strongly influenced by both intraguild competition and predation. However, intraguild interactions involving the world’s most common carnivore, the domestic dog (Canis familiaris), have rarely been investigated. We experimentally examined the behavioural responses of a small canid, the Indian fox (Vulpes bengalensis), to the presence of dogs and dog odours. Resource competition between dogs and Indian foxes is low, so it is unclear whether foxes perceive dogs as interference competitors. To test this, we exposed foxes to neutral, live dog, and animal odour stimuli at food trays, and recorded the time spent at food trays, the amount of food eaten, and vigilance and non-vigilance behaviours. When dogs were visible, foxes continued to visit the food trays, but reduced the amount of time spent and food eaten at those trays. Foxes were more vigilant during dog trials than during neutral and odour trials and also exhibited lower levels of non-vigilance behaviour (resting and playing). In contrast, dog odours did not affect fox foraging and activity. These results show that vigilance/foraging trade-offs due to interference competition can occur between native and domestic carnivores despite low dietary overlap. These negative effects of dogs on a smaller member of the carnivore guild raise conservation concerns, especially for endangered carnivores. In many parts of the world, free-ranging dog densities are high due to human subsidies, and these subsidized predators have the potential to exacerbate the indirect effects of human presence.     

Demography of central and marginal populations of monkeyflowers (Mimulus cardinalis and M. lewisii)

Every species occupies a limited geographic area, but how spatiotemporal environmental variation affects individual and population fitness to create range limits is not well understood. Because range boundaries arise where, on average, populations are more likely to go extinct than to persist, range limits are an inherently population-level problem for which a demographic framework is useful. In this study, I compare demographic parameters and population dynamics between central and marginal populations of monkeyflowers, Mimulus cardinalis and M. lewisii, along an elevation gradient spanning both species' ranges. Central and marginal populations of both species differed in survival and fecundity. For M. lewisii, these components of fitness were higher in central than in marginal populations, but for M. cardinalis the converse was true. To assess spatiotemporal variation in population dynamics, I used transition matrix models to estimate asymptotic population growth rates (lambda) and found that population growth rates of M. lewisii were highest at the range center and reduced at the range margin. Population growth rates of M. cardinalis were highest at the range margin and greatly reduced at the range center. Life table response analysis decomposed spatiotemporal variation in lambda into contributions from each transition between life stages, finding that transitions from large nonreproductive and reproductive plants to the seed class and stasis in the reproductive class made the largest contributions to spatial differences in lambda. These transitions had only low to moderate sensitivities, indicating that differences in projected population growth rates resulted mainly from observed differences in transition matrix parameters and their underlying vital rates.     

Recolonizing wolves and mesopredator suppression of coyotes: impacts on pronghorn population dynamics.

Food web theory predicts that the loss of large carnivores may contribute to elevated predation rates and, hence, declining prey populations, through the process of mesopredator release. However, opportunities to test predictions of the mesopredator release hypothesis are rare, and the extent to which changes in predation rates influence prey population dynamics may not be clear due to a lack of demographic information on the prey population of interest. We utilized spatial and seasonal heterogeneity in wolf distribution and abundance to evaluate whether mesopredator release of coyotes (Canis latrans), resulting from the extirpation of wolves (Canis lupus) throughout much of the United States, contributes to high rates of neonatal mortality in ungulates. To test this hypothesis, we contrasted causes of mortality and survival rates of pronghorn (Antilocapra americana) neonates captured at wolf-free and wolf-abundant sites in western Wyoming, USA, between 2002 and 2004. We then used these data to parameterize stochastic population models to heuristically assess the impact of wolves on pronghorn population dynamics due to changes in neonatal survival. Coyote predation was the primary cause of mortality at all sites, but mortality due to coyotes was 34% lower in areas utilized by wolves (P < 0.001). Based on simulation modeling, the realized population growth rate was 0.92 based on fawn survival in the absence of wolves, and 1.06 at sites utilized by wolves. Thus, wolf restoration is predicted to shift the trajectory of the pronghorn population from a declining to an increasing trend. Our results suggest that reintroductions of large carnivores may influence biodiversity through effects on prey populations mediated by mesopredator suppression. In addition, our approach, which combines empirical data on the population of interest with information from other data sources, demonstrates the utility of using simulation modeling to more fully evaluate ecological theories by moving beyond estimating changes in vital rates to analyses of population-level impacts.     

Rats on the run: removal of alien terrestrial predators affects bush rat behaviour

Predators can strongly influence the microhabitat use and foraging behaviour of prey. In a large-scale replicated field experiment in East Gippsland, Australia, we tested the effects of reduced alien red fox (Vulpes vulpes) and alien wild dog (Canis lupus familiaris) abundance (treatment) on native bush rat (Rattus fuscipes) behaviour. Bush rats are exposed to two main guilds of predators, namely mammalian carnivores and birds of prey. Tracking rat movements using the spool-and-line technique revealed that, in treatment sites, rats used ground cover, which provides shelter from predators, less often than at unmanipulated fox and wild dog abundance (non-treatment sites). In treatment sites, rats more frequently moved on logs where they would have been exposed to hunting foxes and dogs than in non-treatment sites. Furthermore, in treatments, rats showed a preference for understorey but not in non-treatments. Hence, bush rats adapted their behaviour to removal of alien terrestrial predators. Giving-up densities (GUDs) indicated no treatment effects on the marginal feeding rate of bush rats. Interestingly, GUDs were higher in open patches than in sheltered patches, suggesting higher perceived predation risk of bush rats during foraging at low versus high cover. The lack of treatment effects on GUDs but the clear response of bush rats to cover may be explained by the impact of predators other than foxes and wild dogs.     

Golden Eagle fatalities and the continental‐scale consequences of local wind‐energy generation

Renewable energy production is expanding rapidly despite mostly unknown environmental effects on wildlife and habitats. We used genetic and stable isotope data collected from Golden Eagles (Aquila chrysaetos) killed at the Altamont Pass Wind Resource Area (APWRA) in California in demographic models to test hypotheses about the geographic extent and demographic consequences of fatalities caused by renewable energy facilities. Geospatial analyses of δ²H values obtained from feathers showed that ≥25% of these APWRA‐killed eagles were recent immigrants to the population, most from long distances away (>100 km). Data from nuclear genes indicated this subset of immigrant eagles was genetically similar to birds identified as locals from the δ²H data. Demographic models implied that in the face of this mortality, the apparent stability of the local Golden Eagle population was maintained by continental‐scale immigration. These analyses demonstrate that ecosystem management decisions concerning the effects of local‐scale renewable energy can have continental‐scale consequences.     

Investigating Potential for Depensation in Marine Turtles: How Low Can You Go?

Abstract:  Where mechanisms inherent within the biology of a species affect individual fitness at low density, demographic-scale depensation may occur, hastening further decline and leading ultimately to population extirpation and species extinction. Reduction in fertility at low population densities has been identified in marine and terrestrial species. Using data on hatch success and hatchling-emergence success as proxies for fertilization success, we conducted a global meta-analysis of data from breeding aggregations of green turtles ( Chelonia mydas ) and loggerhead turtles ( Caretta caretta ). We found that there has been no reduction in fertility in small nesting aggregations in either of these species worldwide. We considered mechanisms within the mating strategies and reproductive biology of marine turtles that may allow for novel genetic input and facilitate enhanced gene flow among rookeries. Behavioral reproductive mechanisms, such as natal philopatry and polyandry, may mitigate potential impacts of depensation and contribute to the resilience of these species.     

Modulation of predator-prey interactions by the Allee effect

An Allee effect arising from density-dependent mating success can have significant impacts at the ecosystem level when considered in the context of predator-prey interactions. These are captured by a mathematical model for the exchange of biomass between a structured predator population (continuous weight distribution) and a resource. Because the predator’s mating success affects the amount of resources required for the production of offsprings and their future growth into mature organisms, it influences the flux of biomass between trophic levels. Under simple assumptions, the equations can be reduced to an equivalent unstructured predator-prey model in which the Allee effect modulates the predation rate: the mating probability multiplies the rate of predator growth as well as the rate of resource depletion. Implications of the Allee effect for the bifurcation structure and equilibrium densities are examined. The model is compared to a modified version in which the Allee effect instead modulates the assimilation efficiency, hence the mating probability does not appear in the dynamical equation for the resource density. Both models exhibit qualitatively similar dynamics. However, compared to the model in which the Allee effect modulates predation, the model in which the Allee effect modulates assimilation efficiency predicts (i) unrealistically inefficient resource assimilation when predator density is low, (ii) a higher risk of catastrophic extinction resulting from a change in the parameter controlling the strength of the Allee effect, and (iii) no possibility of an increase in population size when the density dependence is enhanced.     

The consequences of being colonial: Allee effects in metapopulations of seabirds

Most seabirds live in large colonies. This fact signifies that there is an advantage in living and breeding together. Four explanations are put fore ward for this colonial behaviour, more birds have: (1) a reduced per capita predation of chicks in colonies, (2) a better anti-predator defence, (3) a more efficient foraging in temporally patchy environments and (4) sex ratios that are more likely to be close to one. These factors induce a strong Allee-type density-dependent relation, a positive relation between density and population growth rate at low density. Nevertheless, these Allee effects are generally ignored in seabird population studies. Therefore we study the consequences of introducing Allee-type density-dependent relations in a spatially explicit metapopulation model for the Common Tern (Sterna hirundo). Simulations show that Allee effects might be responsible for a 20-fold decline in the recolonization distances, causing patches and parts of metapopulations to effectively become more isolated. This leads to long recolonization times of empty breeding patches which consequently cause slower metapopulation expansion and recovery. Additionally, we show that the typical early warning signals, that show that a population is near its critical threshold induce by Allee effects, is less pronounced in colonies that are part of a metapopulation. Hence, we offer some simple equations to estimate critical densities and thresholds in a colony.