Inferring the nature of anthropogenic threats from long‐term abundance records

Diagnosing the processes that threaten species persistence is critical for recovery planning and risk forecasting. Dominant threats are typically inferred by experts on the basis of a patchwork of informal methods. Transparent, quantitative diagnostic tools would contribute much‐needed consistency, objectivity, and rigor to the process of diagnosing anthropogenic threats. Long‐term census records, available for an increasingly large and diverse set of taxa, may exhibit characteristic signatures of specific threatening processes and thereby provide information for threat diagnosis. We developed a flexible Bayesian framework for diagnosing threats on the basis of long‐term census records and diverse ancillary sources of information. We tested this framework with simulated data from artificial populations subjected to varying degrees of exploitation and habitat loss and several real‐world abundance time series for which threatening processes are relatively well understood: bluefin tuna (Thunnus maccoyii) and Atlantic cod (Gadus morhua) (exploitation) and Red Grouse (Lagopus lagopus scotica) and Eurasian Skylark (Alauda arvensis) (habitat loss). Our method correctly identified the process driving population decline for over 90% of time series simulated under moderate to severe threat scenarios. Successful identification of threats approached 100% for severe exploitation and habitat loss scenarios. Our method identified threats less successfully when threatening processes were weak and when populations were simultaneously affected by multiple threats. Our method selected the presumed true threat model for all real‐world case studies, although results were somewhat ambiguous in the case of the Eurasian Skylark. In the latter case, incorporation of an ancillary source of information (records of land‐use change) increased the weight assigned to the presumed true model from 70% to 92%, illustrating the value of the proposed framework in bringing diverse sources of information into a common rigorous framework. Ultimately, our framework may greatly assist conservation organizations in documenting threatening processes and planning species recovery. Inferencia la Naturaleza de las Amenazas Antropogénicas para los Registros de Abundancia a Largo Plazo     

Range‐Wide Genetic Connectivity of the Hawaiian Monk Seal and Implications for Translocation

Abstract: The Hawaiian monk seal (Monachus schauinslandi) is one of the most critically endangered marine mammals. Less than 1200 individuals remain, and the species is declining at a rate of approximately 4% per year as a result of juvenile starvation, shark predation, and entanglement in marine debris. Some of these problems may be alleviated by translocation; however, if island breeding aggregates are effectively isolated subpopulations, moving individuals may disrupt local adaptations. In these circumstances, managers must balance the pragmatic need of increasing survival with theoretical concerns about genetic viability. To assess range‐wide population structure of the Hawaiian monk seal, we examined an unprecedented, near‐complete genetic inventory of the species (n =1897 seals, sampled over 14 years) at 18 microsatellite loci. Genetic variation was not spatially partitioned (_w=?0.03, p = 1.0), and a Bayesian clustering method provided evidence of one panmictic population (K =1). Pairwise F_ST comparisons (among 7 island aggregates over 14 annual cohorts) did not reveal temporally stable, spatial reproductive isolation. Our results coupled with long‐term tag‐resight data confirm seal movement and gene flow throughout the Hawaiian Archipelago. Thus, human‐mediated translocation of seals among locations is not likely to result in genetic incompatibilities.     

Effects of Amphibian Chytrid Fungus on Individual Survival Probability in Wild Boreal Toads

Abstract: Chytridiomycosis is linked to the worldwide decline of amphibians, yet little is known about the demographic effects of the disease. We collected capture–recapture data on three populations of boreal toads (Bufo boreas [Bufo = Anaxyrus]) in the Rocky Mountains (U.S.A.). Two of the populations were infected with chytridiomycosis and one was not. We examined the effect of the presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]; the agent of chytridiomycosis) on survival probability and population growth rate. Toads that were infected with Bd had lower average annual survival probability than uninfected individuals at sites where Bd was detected, which suggests chytridiomycosis may reduce survival by 31–42% in wild boreal toads. Toads that were negative for Bd at infected sites had survival probabilities comparable to toads at the uninfected site. Evidence that environmental covariates (particularly cold temperatures during the breeding season) influenced toad survival was weak. The number of individuals in diseased populations declined by 5–7%/year over the 6 years of the study, whereas the uninfected population had comparatively stable population growth. Our data suggest that the presence of Bd in these toad populations is not causing rapid population declines. Rather, chytridiomycosis appears to be functioning as a low‐level, chronic disease whereby some infected individuals survive but the overall population effects are still negative. Our results show that some amphibian populations may be coexisting with Bd and highlight the importance of quantitative assessments of survival in diseased animal populations.     

Use of Spatial Capture‐Recapture Modeling and DNA Data to Estimate Densities of Elusive Animals

Abstract: Assessment of abundance, survival, recruitment rates, and density (i.e., population assessment) is especially challenging for elusive species most in need of protection (e.g., rare carnivores). Individual identification methods, such as DNA sampling, provide ways of studying such species efficiently and noninvasively. Additionally, statistical methods that correct for undetected animals and account for locations where animals are captured are available to efficiently estimate density and other demographic parameters. We collected hair samples of European wildcat (Felis silvestris) from cheek‐rub lure sticks, extracted DNA from the samples, and identified each animals’ genotype. To estimate the density of wildcats, we used Bayesian inference in a spatial capture‐recapture model. We used WinBUGS to fit a model that accounted for differences in detection probability among individuals and seasons and between two lure arrays. We detected 21 individual wildcats (including possible hybrids) 47 times. Wildcat density was estimated at 0.29/km² (SE 0.06), and 95% of the activity of wildcats was estimated to occur within 1.83 km from their home‐range center. Lures located systematically were associated with a greater number of detections than lures placed in a cell on the basis of expert opinion. Detection probability of individual cats was greatest in late March. Our model is a generalized linear mixed model; hence, it can be easily extended, for instance, to incorporate trap‐ and individual‐level covariates. We believe that the combined use of noninvasive sampling techniques and spatial capture‐recapture models will improve population assessments, especially for rare and elusive animals.     

A Framework for Developing Objective and Measurable Recovery Criteria for Threatened and Endangered Species

For species listed under the U.S. Endangered Species Act (ESA), the U.S. Fish and Wildlife Service and National Marine Fisheries Service are tasked with writing recovery plans that include “objective, measurable criteria” that define when a species is no longer at risk of extinction, but neither the act itself nor agency guidelines provide an explicit definition of objective, measurable criteria. Past reviews of recovery plans, including one published in 2012, show that many criteria lack quantitative metrics with clear biological rationale and are not meeting the measureable and objective mandate. I reviewed how objective, measureable criteria have been defined implicitly and explicitly in peer‐reviewed literature, the ESA, other U.S. statutes, and legal decisions. Based on a synthesis of these sources, I propose the following 6 standards be used as minimum requirements for objective, measurable criteria: contain a quantitative threshold with calculable units, stipulate a timeframe over which they must be met, explicitly define the spatial extent or population to which they apply, specify a sampling procedure that includes sample size, specify a statistical significance level, and include justification by providing scientific evidence that the criteria define a species whose extinction risk has been reduced to the desired level. To meet these 6 standards, I suggest that recovery plans be explicitly guided by and organized around a population viability modeling framework even if data or agency resources are too limited to complete a viability model. When data and resources are available, recovery criteria can be developed from the population viability model results, but when data and resources are insufficient for model implementation, extinction risk thresholds can be used as criteria. A recovery‐planning approach centered on viability modeling will also yield appropriately focused data‐acquisition and monitoring plans and will facilitate a seamless transition from recovery planning to delisting. Un Marco de Referencia para Desarrollar Criterios de Recuperación Objetivos y Medibles para Especies Amenazadas y en Peligro     

Inbreeding Depression Accumulation across Life‐History Stages of the Endangered Takahe

Abstract: Studies evaluating the impact of inbreeding depression on population viability of threatened species tend to focus on the effects of inbreeding at a single life‐history stage (e.g., juvenile survival). We examined the effects of inbreeding across the full life‐history continuum, from survival up to adulthood, to subsequent reproductive success, and to the recruitment of second‐generation offspring, in wild Takahe ( Porphyrio hochstetteri ) by analyzing pedigree and fitness data collected over 21 breeding seasons. Although the effect size of inbreeding at individual life‐history stages was small, inbreeding depression accumulated across multiple life‐history stages and ultimately reduced long‐term fitness (i.e., successful recruitment of second‐generation offspring). The estimated total lethal equivalents (2B) summed across all life‐history stages were substantial (16.05, 95% CI 0.08–90.8) and equivalent to an 88% reduction in recruitment of second‐generation offspring for closely related pairs (e.g., sib–sib pairings) relative to unrelated pairs (according to the pedigree). A history of small population size in the Takahe could have contributed to partial purging of the genetic load and the low level of inbreeding depression detected at each single life‐history stage. Nevertheless, our results indicate that such “purged” populations can still exhibit substantial inbreeding depression, especially when small but negative fitness effects accumulate across the species’ life history. Because inbreeding depression can ultimately affect population viability of small, isolated populations, our results illustrate the importance of measuring the effects of inbreeding across the full life‐history continuum.     

Revealing life‐history traits by contrasting genetic estimations with predictions of effective population size

Effective population size, a central concept in conservation biology, is now routinely estimated from genetic surveys and can also be theoretically predicted from demographic, life‐history, and mating‐system data. By evaluating the consistency of theoretical predictions with empirically estimated effective size, insights can be gained regarding life‐history characteristics and the relative impact of different life‐history traits on genetic drift. These insights can be used to design and inform management strategies aimed at increasing effective population size. We demonstrated this approach by addressing the conservation of a reintroduced population of Asiatic wild ass (Equus hemionus). We estimated the variance effective size (N_ev) from genetic data () and formulated predictions for the impacts on N_ev of demography, polygyny, female variance in lifetime reproductive success (RS), and heritability of female RS. By contrasting the genetic estimation with theoretical predictions, we found that polygyny was the strongest factor affecting genetic drift because only when accounting for polygyny were predictions consistent with the genetically measured N_ev. The comparison of effective‐size estimation and predictions indicated that 10.6% of the males mated per generation when heritability of female RS was unaccounted for (polygyny responsible for 81% decrease in N_ev) and 19.5% mated when female RS was accounted for (polygyny responsible for 67% decrease in N_ev). Heritability of female RS also affected N_ev; (heritability responsible for 41% decrease in N_ev). The low effective size is of concern, and we suggest that management actions focus on factors identified as strongly affecting , namely, increasing the availability of artificial water sources to increase number of dominant males contributing to the gene pool. This approach, evaluating life‐history hypotheses in light of their impact on effective population size, and contrasting predictions with genetic measurements, is a general, applicable strategy that can be used to inform conservation practice.     

Effects of Growth Form and Functional Traits on Response of Woody Plants to Clearing and Fragmentation of Subtropical Rainforest

The conservation implications of large‐scale rainforest clearing and fragmentation on the persistence of functional and taxonomic diversity remain poorly understood. If traits represent adaptive strategies of plant species to particular circumstances, the expectation is that the effect of forest clearing and fragmentation will be affected by species functional traits, particularly those related to dispersal. We used species occurrence data for woody plants in 46 rainforest patches across 75,000 ha largely cleared of forest by the early 1900s to determine the combined effects of area reduction, fragmentation, and patch size on the taxonomic structure and functional diversity of subtropical rainforest. We compiled species trait values for leaf area, seed dry mass, wood density, and maximum height and calculated species niche breadths. Taxonomic structure, trait values (means, ranges), and the functional diversity of assemblages of climbing and free‐standing plants in remnant patches were quantified. Larger rainforest patches had higher species richness. Species in smaller patches were taxonomically less related than species in larger patches. Free‐standing plants had a high percentage of frugivore dispersed seeds; climbers had a high proportion of small wind‐dispersed seeds. Connections between the patchy spatial distribution of free‐standing species, larger seed sizes, and dispersal syndrome were weak. Assemblages of free‐standing plants in patches showed more taxonomic and spatial structuring than climbing plants. Smaller isolated patches retained relatively high functional diversity and similar taxonomic structure to larger tracts of forest despite lower species richness. The response of woody plants to clearing and fragmentation of subtropical rainforest differed between climbers and slow‐growing mature‐phase forest trees but not between climbers and pioneer trees. Quantifying taxonomic structure and functional diversity provides an improved basis for conservation planning and management by elucidating the effects of forest‐area reduction and fragmentation. Efectos de la Forma de Crecimiento y Atributos Funcionales en la Respuesta de Plantas Leñosas al Desmonte y Fragmentación de Bosque Lluvioso Subtropical     

Targeted gene flow and rapid adaptation in an endangered marsupial

Targeted gene flow is an emerging conservation strategy. It involves translocating individuals with favorable genes to areas where they will have a conservation benefit. The applications for targeted gene flow are wide-ranging but include preadapting native species to the arrival of invasive species. The endangered carnivorous marsupial, the northern quoll (Dasyurus hallucatus), has declined rapidly since the introduction of the cane toad (Rhinella marina), which fatally poisons quolls that attack them. There are, however, a few remaining toad-invaded quoll populations in which the quolls survive because they know not to eat cane toads. It is this toad-smart behavior we hope to promote through targeted gene flow. For targeted gene flow to be feasible, however, toad-smart behavior must have a genetic basis. To assess this, we used a common garden experiment, comparing offspring from toad-exposed and toad-naïve parents raised in identical environments, to determine whether toad-smart behavior is heritable. Offspring from toad-exposed populations were substantially less likely to eat toads than those with toad-naïve parents. Hybrid offspring showed similar responses to quolls with 2 toad-exposed parents, indicating the trait may be dominant. Together, these results suggest a heritable trait and rapid adaptive response in a small number of toad-exposed populations. Although questions remain about outbreeding depression, our results are encouraging for targeted gene flow. It should be possible to introduce toad-smart behavior into soon to be affected quoll populations.     

Effects of learning and adaptation on population viability

Cultural adaptation is one means by which conservationists may help populations adapt to threats. A learned behavior may protect an individual from a threat, and the behavior can be transmitted horizontally (within generations) and vertically (between generations), rapidly conferring population-level protection. Although possible in theory, it remains unclear whether such manipulations work in a conservation setting; what conditions are required for them to work; and how they might affect the evolutionary process. We examined models in which a population can adapt through both genetic and cultural mechanisms. Our work was motivated by the invasion of highly toxic cane toads (Rhinella marina) across northern Australia and the resultant declines of endangered northern quolls (Dasyurus hallucatus), which attack and are fatally poisoned by the toxic toads. We examined whether a novel management strategy in which wild quolls are trained to avoid toads can reduce extinction probability. We used a simulation model tailored to quoll life history. Within simulations, individuals were trained and a continuous evolving trait determined innate tendency to attack toads. We applied this model in a population viability setting. The strategy reduced extinction probability only when heritability of innate aversion was low (<20%) and when trained mothers trained >70% of their young to avoid toads. When these conditions were met, genetic adaptation was slower, but rapid cultural adaptation kept the population extant while genetic adaptation was completed. To gain insight into the evolutionary dynamics (in which we saw a transitory peak in cultural adaptation over time), we also developed a simple analytical model of evolutionary dynamics. This model showed that the strength of natural selection declined as the cultural transmission rate increased and that adaptation proceeded only when the rate of cultural transmission was below a critical value determined by the relative levels of protection conferred by genetic versus cultural mechanisms. Together, our models showed that cultural adaptation can play a powerful role in preventing extinction, but that rates of cultural transmission need to be high for this to occur.