Heterozygosity‐Fitness Correlations and Inbreeding Depression in Two Critically Endangered Mammals

The relation among inbreeding, heterozygosity, and fitness has been studied primarily among outbred populations, and little is known about these phenomena in endangered populations. Most researchers conclude that the relation between coefficient of inbreeding estimated from pedigrees and fitness traits (inbreeding‐fitness correlations) better reflects inbreeding depression than the relation between marker heterozygosity and fitness traits (heterozygosity‐fitness correlations). However, it has been suggested recently that heterozygosity‐fitness correlations should only be expected when inbreeding generates extensive identity disequilibrium (correlations in heterozygosity and homozygosity across loci throughout the genome). We tested this hypothesis in Mohor gazelle (Gazella dama mhorr) and Iberian lynx (Lynx pardinus). For Mohor gazelle, we calculated the inbreeding coefficient and measured heterozygosity at 17 microsatellite loci. For Iberian lynx, we measured heterozygosity at 36 microsatellite loci. In both species we estimated semen quality, a phenotypic trait directly related to fitness that is controlled by many loci and is affected by inbreeding depression. Both species showed evidence of extensive identity disequilibrium, and in both species heterozygosity was associated with semen quality. In the Iberian lynx the low proportion of normal sperm associated with low levels of heterozygosity was so extreme that it is likely to limit the fertility of males. In Mohor gazelle, although heterozygosity was associated with semen quality, inbreeding coefficient was not. This result suggests that when coefficient of inbreeding is calculated on the basis of a genealogy that begins after a long history of inbreeding, the coefficient of inbreeding fails to capture previous demographic information because it is a poor estimator of accumulated individual inbreeding. We conclude that among highly endangered species with extensive identity disequilibrium, examination of heterozygosity‐fitness correlations may be an effective way to detect inbreeding depression, whereas inbreeding‐fitness correlations may be poor indicators of inbreeding depression if the pedigree does not accurately reflect the history of inbreeding. Correlaciones Heterocigosidad‐ Adaptabilidad y Depresión Endogámica en Dos Especies de Mamíferos Críticamente en Peligro     

Effect of Macroalgal Expansion and Marine Protected Areas on Coral Recovery Following a Climatic Disturbance

Disturbance plays an important role in structuring marine ecosystems, and there is a need to understand how conservation practices, such as the designation of Marine Protected Areas (MPAs), facilitate postdisturbance recovery. We evaluated the association of MPAs, herbivorous fish biomass, substrate type, postdisturbance coral cover, and change in macroalgal cover with coral recovery on the fringing reefs of the inner Seychelle islands, where coral mortality after a 1998 bleaching event was extensive. We visually estimated benthic cover and fish biomass at 9 sites in MPAs where fishing is banned and at 12 sites where fishing is permitted in 1994, 2005, 2008, and 2011. We used analysis of variance to examine spatial and temporal variations in coral cover and generalized additive models to identify relations between coral recovery and the aforementioned factors that may promote recovery. Coral recovery occurred on all substrate types, but it was highly variable among sites and times. Between 2005 and 2011 the increase in coral cover averaged 1%/year across 21 sites, and the maximum increase was 4%/year. However, mean coral cover across the study area (14%) remained at half of 1994 levels (28%). Sites within MPAs had faster rates of coral recovery than sites in fished areas only where cover of macroalgae was low and had not increased over time. In MPAs where macroalgae cover expanded since 1998 there was no recovery. Where coral was recovering on granite reefs there was a shift in relative prevalence of colony life‐form from branching to encrusting species. This simplification of reef structure may affect associated reef fauna even if predisturbance levels of coral cover are attained. Efecto de la Expansión de Macroalgas y Áreas Marinas Protegidas sobre la Recuperación de Coral Después de una Perturbación Climática     

Decision‐Making Triggers in Adaptive Management

We analyzed whether decision‐making triggers increase accountability of adaptive‐management plans. Triggers are prenegotiated commitments in an adaptive‐management plan that specify what actions are to be taken and when on the basis of information obtained from monitoring. Triggers improve certainty that particular actions will be taken by agencies in the future. We conducted an in‐depth, qualitative review of the political and legal contexts of adaptive management and its application by U.S. federal agencies. Agencies must satisfy the judiciary that adaptive‐management plans meet substantive legal standards and comply with the U.S. National Environmental Policy Act. We examined 3 cases in which triggers were used in adaptive‐management plans: salmon (Oncorhynchus spp.) in the Columbia River, oil and gas development by the Bureau of Land Management, and a habitat conservation plan under the U.S. Endangered Species Act. In all the cases, key aspects of adaptive management, including controls and preidentified feedback loops, were not incorporated in the plans. Monitoring and triggered mitigation actions were limited in their enforceability, which was contingent on several factors, including which laws applied in each case and the degree of specificity in how triggers were written into plans. Other controversial aspects of these plans revolved around who designed, conducted, interpreted, and funded monitoring programs. Additional contentious issues were the level of precaution associated with trigger mechanisms and the definition of ecological baselines used as points of comparison. Despite these challenges, triggers can be used to increase accountability, by predefining points at which an adaptive management plan will be revisited and reevaluated, and thus improve the application of adaptive management in its complicated political and legal context. Detonadores de la Toma de Decisiones en el Manejo Adaptativo     

Interacting Effects of Translocation,Artificial Propagation,and Environmental Conditions on the Marine Survival of Chinook Salmon from the Columbia River,Washington, U.S.A.

Abstract: Captive rearing and translocation are often used concurrently for species conservation, yet the effects of these practices can interact and lead to unintended outcomes that may undermine species’ recovery efforts. Controls in translocation or artificial‐propagation programs are uncommon; thus, there have been few studies on the interacting effects of these actions and environmental conditions on survival. The Columbia River basin, which drains 668,000 km² of the western United States and Canada, has an extensive network of hydroelectric and other dams, which impede and slow migration of anadromous Pacific salmon (Oncorhynchus spp.) and can increase mortality rates. To mitigate for hydrosystem‐induced mortality during juvenile downriver migration, tens of millions of hatchery fish are released each year and a subset of wild‐ and hatchery‐origin juveniles are translocated downstream beyond the hydropower system. We considered how the results of these practices interact with marine environmental conditions to affect the marine survival of Chinook salmon (O. tshawytscha). We analyzed data from more than 1 million individually tagged fish from 1998 through 2006 to evaluate the probability of an individual fish returning as an adult relative to its rearing (hatchery vs. wild) and translocation histories (translocated vs. in‐river migrating fish that traveled downriver through the hydropower system) and a suite of environmental variables. Except during select periods of very low river flow, marine survival of wild translocated fish was approximately two‐thirds less than survival of wild in‐river migrating fish. For hatchery fish, however, survival was roughly two times higher for translocated fish than for in‐river migrants. Competition and predator aggregation negatively affected marine survival, and the magnitude of survival depended on rearing and translocation histories and biological and physical conditions encountered during their first few weeks of residence in the ocean. Our results highlight the importance of considering the interacting effects of translocation, artificial propagation, and environmental variables on the long‐term viability of species.     

Role of Familiarity and Preference in Reproductive Success in Ex Situ Breeding Programs

Abstract: Success of captive‐breeding programs centers on consistent reproduction among captive animals. However, many individuals do not reproduce even when they are apparently healthy and presented with mates. Mate choice can affect multiple parameters of reproductive success, including mating success, offspring production, offspring survival, and offspring fecundity. We investigated the role of familiarity and preference on reproductive success of female Columbia Basin pygmy rabbits (Brachylagus idahoensis) as measured by litter production, litter size, average number of young that emerged from the burrow, and average number of young that survived to 1 year. We conducted these studies on pygmy rabbits at the Oregon Zoo (Portland, Oregon, U.S.A.) and Washington State University (Pullman, Washington, U.S.A.) from February to June 2006, 2007, and 2008. Before mating, we housed each female adjacent to 2 males (neighbors). Female preference for each potential mate was determined on the basis of behavioral interactions observed and measured between the rabbits. We compared reproductive success between females mated with neighbor and non‐neighbor males and between females mated with preferred and nonpreferred males. Our findings suggest that mating with a neighbor compared with a non‐neighbor and mating with a preferred neighbor compared with a nonpreferred neighbor increased reproductive success in female pygmy rabbits. Litter production, average number of young that emerged, and average number of young that survived to 1 year were higher in rabbits that were neighbors before mating than in animals who were not neighbors. Pairing rabbits with a preferred partner increased the probability of producing a litter and was significantly associated with increased litter size. In captive breeding programs, mates are traditionally selected on the basis of genetic parameters to minimize loss of genetic diversity and inbreeding coefficients. Our results suggest that integrating genetic information with social dynamics and behavioral measures of preference may increase the reproductive output of the pygmy rabbit captive‐breeding program. Our findings are consistent with the idea that allowing mate choice and familiarity increase the reproductive success of captive‐breeding programs for endangered species.     

Using ecosystem-services assessments to determine trade-offs in ecosystem-based management of marine mammals

The goal of ecosystem-based management (EBM) is to support a sustainable and holistic multisectored management approach, and is recognized in a number of international policy frameworks. However, it remains unknown how these goals should be linked to assessments and management plans for marine fauna, such as mammals and fish stocks. It appears particularly challenging to carry out trade-off analyses of various ocean uses without a framework that integrates knowledge of environmental, social, and economic benefits derived from nonstationary marine fauna. We argue this gap can be filled by applying a version of the ecosystem-service approach at the population level of marine fauna. To advance this idea, we used marine mammals as a case study to demonstrate what indicators could operationalize relevant assessments and deliver an evidence base for the presence of ecosystem services and disservices derived from marine mammals. We found indicators covering common ecosystem service categories feasible to apply; examples of indicator data are already available in the literature for several populations. We encourage further exploration of this approach for application to marina fauna and biodiversity management, with the caveat that conceptual tensions related to the use of the ecosystem service concept itself needs to be addressed to ensure acceptance by relevant stakeholders.     

An ecological framework for contextualizing carnivore–livestock conflict

Carnivore predation on livestock is a complex management and policy challenge, yet it is also intrinsically an ecological interaction between predators and prey. Human–wildlife interactions occur in socioecological systems in which human and environmental processes are closely linked. However, underlying human–wildlife conflict and key to unpacking its complexity are concrete and identifiable ecological mechanisms that lead to predation events. To better understand how ecological theory accords with interactions between wild predators and domestic prey, we developed a framework to describe ecological drivers of predation on livestock. We based this framework on foundational ecological theory and current research on interactions between predators and domestic prey. We used this framework to examine ecological mechanisms (e.g., density-mediated effects, behaviorally mediated effects, and optimal foraging theory) through which specific management interventions operate, and we analyzed the ecological determinants of failure and success of management interventions in 3 case studies: snow leopards (Panthera uncia), wolves (Canis lupus), and cougars (Puma concolor). The varied, context-dependent successes and failures of the management interventions in these case studies demonstrated the utility of using an ecological framework to ground research and management of carnivore–livestock conflict. Mitigation of human–wildlife conflict appears to require an understanding of how fundamental ecological theories work within domestic predator–prey systems.     

A critical appraisal of population viability analysis

Population viability analysis (PVA) is useful in management of imperiled species. Applications range from research design, threat assessment, and development of management frameworks. Given the importance of PVAs, it is essential that they be rigorous and adhere to widely accepted guidelines; however, the quality of published PVAs is rarely assessed. We evaluated the quality of 160 PVAs of 144 species of birds and mammals published in peer-reviewed journals from 1990 to 2017. We hypothesized that PVA quality would be lower with generic programs than with custom-built programs; be higher for those developed for imperiled species; change over time; and be higher for those published in journals with high impact factors (IFs). Each included study was evaluated based on answers to an evaluation framework containing 32 questions reflecting whether and to what extent the PVA study adhered to published PVA guidelines or contained important PVA components. All measures of PVA quality were generally lower for studies based on generic programs. Conservation status of the species did not affect any measure of PVA quality, but PVAs published in high IF journals were of higher quality. Quality generally declined over time, suggesting the quantitative literacy of PVA practitioners has not increased over time or that PVAs developed by unskilled users are being published in peer-reviewed journals. Only 18.1% of studies were of high quality (score >75%), which is troubling because poor-quality PVAs could misinform conservation decisions. We call for increased scrutiny of PVAs by journal editors and reviewers. Our evaluation framework can be used for this purpose. Because poor-quality PVAs continue to be published, we recommend caution while using PVA results in conservation decision making without thoroughly assessing the PVA quality.     

Species Listing under Canada's Species at Risk Act

Abstract: In a preliminary analysis of listing decisions under Canada's Species at Risk Act (SARA), Mooers et al. (2007) demonstrated an apparent bias against marine and northern species. As a follow‐up, we expanded the set of potential explanatory variables, including information on jurisdictional and administrative elements of the listing process, and considered an additional 16 species recommended for listing by SARA's scientific advisory committee as of 15 August 2006. Logistic model selection based on Akaike differences suggested that species were less likely to be listed if they were harvested or had commercial or subsistence harvesting as an explicitly identified threat; had Department of Fisheries and Oceans (DFO) as a responsible authority (RA); were located in Canada's north generally, and especially in Nunavut; or were found mostly or entirely within Canada. Subsequent model validation with an independent set of 50 species for which a listing decision was handed down in December 2007 showed an overall misclassification rate of <0.10, indicating reasonable predictive power. In light of these results, we recommend that RAs under SARA adopt a two‐track listing approach to address problems of delays arising from extended consultations and the inconsistent use by the RAs of socioeconomic analysis; consider revising SARA so that socioeconomic analysis occurs during decisions about protecting species and their habitats rather than at the listing stage; and maintain an integrated database with information on species’ biology, threats, and agency actions to enable future evaluation of SARA's impact.     

Use of Surrogates to Predict the Stressor Response of Imperiled Species

Abstract: Rare or narrowly distributed species may be threatened by stressors to which they have never been exposed or for which data are very limited. In such cases the species response cannot be predicted on the basis of directly measured data, but may be inferred from the response of one or more appropriate surrogate species. Here, I propose a practical way to use the stressor response of one or more surrogate species to develop a working hypothesis or model of the stressor response of the target species. The process has 4 steps: (1) identify one or more candidate surrogate species, (2) model the relationship between the stressor and the response variable of interest for the surrogate species, (3) adapt the stressor–response relationship from the surrogate species to a model for the target species, possibly using Bayesian methods, and (4) incorporate additional data as they become available and adjust the response model of the target species appropriately. I applied the approach to an endangered fish species, the amber darter (Percina antesella), which is potentially threatened by urbanization. I used a Bayesian approach to combine data from a surrogate species (the bronze darter[Percina palmaris]) with available data for the amber darter to produce a model of expected amber darter response. Although this approach requires difficult decisions on the part of the manager, especially in the selection of surrogate species, its value lies in the fact that all assumptions are clearly stated in the form of hypotheses, which may be scrutinized and tested. It therefore provides a rational basis for instituting management policy even in the face of considerable uncertainty.