Phenological mismatch and the effectiveness of assisted gene flow

The persistence of narrowly adapted species under climate change will depend on their ability to migrate apace with their historical climatic envelope or to adapt in place to maintain fitness. This second path to persistence can only occur if there is sufficient genetic variance for response to new selection regimes. Inadequate levels of genetic variation can be remedied through assisted gene flow (AGF), that is the intentional introduction of individuals genetically adapted to localities with historic climates similar to the current or future climate experienced by the resident population. However, the timing of reproduction is frequently adapted to local conditions. Phenological mismatch between residents and migrants can reduce resident × migrant mating frequencies, slowing the introgression of migrant alleles into the resident genetic background and impeding evolutionary rescue efforts. Focusing on plants, we devised a method to estimate the frequency of resident × migrant matings based on flowering schedules and applied it in an experiment that mimicked the first generation of an AGF program with Chamaecrista fasciculata, a prairie annual, under current and expected future temperature regimes. Phenological mismatch reduced the potential for resident × migrant matings by 40–90%, regardless of thermal treatment. The most successful migrant sires were the most resident like in their flowering time, further biasing the genetic admixture between resident and migrant populations. Other loci contributing to local adaptation—heat‐tolerance genes, for instance—may be in linkage disequilibrium with phenology when residents and migrants are combined into a single mating pool. Thus, introgression of potentially adaptive migrant alleles into the resident genetic background is slowed when selection acts against migrant phenology. Successful AGF programs may require sustained high immigration rates or preliminary breeding programs when phenologically matched migrant source populations are unavailable.     

Evaluating Alternative Strategies for Minimizing Unintended Fitness Consequences of Cultured Individuals on Wild Populations

Artificial propagation strategies often incur selection in captivity that leads to traits that are maladaptive in the wild. For propagation programs focused on production rather than demographic contribution to wild populations, effects on wild populations can occur through unintentional escapement or the need to release individuals into natural environments for part of their life cycle. In this case, 2 alternative management strategies might reduce unintended fitness consequences on natural populations: (1) reduce selection in captivity as much as possible to reduce fitness load (keep them similar), or (2) breed a separate population to reduce captive‐wild interactions as much as possible (make them different). We quantitatively evaluate these 2 strategies with a coupled demographic–genetic model based on Pacific salmon hatcheries that incorporates a variety of relevant processes and dynamics: selection in the hatchery relative to the wild, assortative mating based on the trait under selection, and different life cycle arrangements in terms of hatchery release, density dependence, natural selection, and reproduction. Model results indicate that, if natural selection only occurs between reproduction and captive release, the similar strategy performs better. However, if natural selection occurs between captive release and reproduction, the different and similar strategies present viable alternatives to reducing unintended fitness consequences because of the greater opportunity to purge maladaptive individuals. In this case, the appropriate approach depends on the feasibility of each strategy and the demographic goal (e.g., increasing natural abundance, or ensuring that a high proportion of natural spawners are naturally produced). In addition, the fitness effects of hatchery release are much greater if hatchery release occurs before (vs. after) density‐dependent interactions. Given the logistical challenges to achieving both the similar and different strategies, evaluation of not just the preferred strategy but also the consequences of failing to achieve the desired target is critical. Evaluación de Estrategias Alternativas para Minimizar las Consecuencias No Inesperadas en la Adecuación de Individuos Criados en Cautiverio sobre Poblaciones Silvestres     

Conflicting and Complementary Ethics of Animal Welfare Considerations in Reintroductions

Despite differences in focus, goals, and strategies between conservation biology and animal welfare, both are inextricably linked in many ways, and greater consideration of animal welfare, although important in its own right, also has considerable potential to contribute to conservation success. Nevertheless, animal welfare and animal ethics are not always considered explicitly within conservation practice. We systematically reviewed the recent scientific peer‐reviewed and online gray literature on reintroductions of captive‐bred and wild‐caught animals (mammals, birds, amphibians, and reptiles) to quantify the occurrence of animal welfare issues. We considered monitoring that could be indicative of the animal's welfare status and supportive management actions that could improve animal welfare (regardless of whether the aim was explicitly animal‐welfare orientated). Potential welfare issues (of variable nature and extent) were recorded in 67% of 199 projects reviewed; the most common were mortality >50%, dispersal or loss of animals, disease, and human conflict. Most (>70%) projects monitored survival, 18% assessed body condition, and 2% monitored stress levels. Animal welfare, explicitly, was referred to in 6% of projects. Supportive actions, most commonly use of on‐site prerelease pens and provision of supplemental food or water, were implemented in 79% of projects, although the extent and duration of support varied. Practitioners can address animal‐welfare issues in reintroductions by considering the potential implications for individual animals at all stages of the release process using the decision tree presented. We urge practitioners to report potential animal‐welfare issues, describe mitigation actions, and evaluate their efficacy to facilitate transparent evaluation of common moral dilemmas and to advance communal strategies for dealing with them. Currently, comparative mortality rates, health risks, postrelease stress, effectiveness of supportive measures, and behavior of individuals warrant further research to improve animal welfare in reintroductions and to increase success of such projects. Ética Conflictiva y Complementaria al Considerar el Bienestar Animal en Reintroducciones     

Challenges and Opportunities in Implementing Managed Relocation for Conservation of Freshwater Species

Abstract: The rapidity of climate change is predicted to exceed the ability of many species to adapt or to disperse to more climatically favorable surroundings. Conservation of these species may require managed relocation (also called assisted migration or assisted colonization) of individuals to locations where the probability of their future persistence may be higher. The history of non‐native species throughout the world suggests managed relocation may not be applicable universally. Given the constrained existence of freshwater organisms within highly dendritic networks containing isolated ponds, lakes, and rivers, managed relocation may represent a useful conservation strategy. Yet, these same distinctive properties of freshwater ecosystems may increase the probability of unintended ecological consequences. We explored whether managed relocation is an ecologically sound conservation strategy for freshwater systems and provided guidelines for identifying candidates and localities for managed relocation. A comparison of ecological and life‐history traits of freshwater animals associated with high probabilities of extirpation and invasion suggests that it is possible to select species for managed relocation to minimize the likelihood of unintended effects to recipient ecosystems. We recommend that translocations occur within the species’ historical range and optimally within the same major river basin and that lacustrine and riverine species be translocated to physically isolated seepage lakes and upstream of natural or artificial barriers, respectively, to lower the risk of secondary spread across the landscape. We provide five core recommendations to enhance the scientific basis of guidelines for managed relocation in freshwater environments: adopt the term managed translocation to reflect the fact that individuals will not always be reintroduced within their historical native range; examine the trade‐off between facilitation of individual movement and the probability of range expansion of non‐native species; determine which species and locations might be immediately considered for managed translocation; adopt a hypothetico‐deductive framework by conducting experimental trials to introduce species of conservation concern into new areas within their historical range; build on previous research associated with species reintroductions through communication and synthesis of case studies.     

A Contemporary,Sex‐Limited Change in Body Size of an Estuarine Turtle in Response to Commercial Fishing

Abstract: Juvenile growth rate and adult body size are important components of life‐history strategies because of their direct impact on fitness. The diamondback terrapin (Malaclemys terrapin) is a sexually dimorphic, long‐lived turtle inhabiting brackish waters throughout the Atlantic and Gulf coasts of the United States. In parts of its range, terrapins face anthropogenically imposed mortality: juveniles of both sexes inadvertently enter commercial crab traps and drown. For adult females, the carapace eventually grows large enough that they cannot enter traps, whereas males almost never reach that critical size. We compared age structure, carapace dimensions, growth curves, and indices of sexual dimorphism for a Chesapeake Bay population of terrapins (where mortality of turtles is high due to crab traps) with contemporary terrapins from Long Island Sound and museum specimens from Chesapeake Bay (neither group subject to commercial crab traps). We also calculated the allochronic and synchronic rates of evolutionary change (haldanes) for males and females to measure the rate of trait change in a population or between populations, respectively. We found a dramatic shift to a younger male age structure, a decrease in the length of time to terminal female carapace size, a 15% increase in female carapace width, and an increase in sexual dimorphism in Chesapeake Bay. In a new twist, our results implicate a fishery in the selective increase in size of a reptilian bycatch species. These sex‐specific changes in life history and demography have implications for population viability that need to be considered when addressing conservation of this threatened turtle.     

Effects of Habitat Fragmentation on Effective Dispersal of Florida Scrub‐Jays

Abstract: Studies comparing dispersal in fragmented versus unfragmented landscapes show that habitat fragmentation alters the dispersal behavior of many species. We used two complementary approaches to explore Florida Scrub‐Jay (Aphelocoma c?rulescens) dispersal in relation to landscape fragmentation. First, we compared dispersal distances of color‐marked individuals in intensively monitored continuous and fragmented landscapes. Second, we estimated effective dispersal relative to the degree of fragmentation (as inferred from two landscape indexes: proportion of study site covered with Florida Scrub‐Jay habitat and mean distance to nearest habitat patch within each study site) by comparing genetic isolation‐by‐distance regressions among 13 study sites having a range of landscape structures. Among color‐banded individuals, dispersal distances were greater in fragmented versus continuous landscapes, a result consistent with other studies. Nevertheless, genetic analyses revealed that effective dispersal decreases as the proportion of habitat in the landscape decreases. These results suggest that although individual Florida Scrub‐Jays may disperse farther as fragmentation increases, those that do so are less successful as breeders than those that disperse short distances. Our study highlights the importance of combining observational data with genetic inferences when evaluating the complex biological and life‐history implications of dispersal.     

The Value of Species and the Ethical Foundations of Assisted Colonization

Abstract: Discourse around assisted colonization focuses on the ecological risks, costs, and uncertainties associated with the practice, as well as on its technical feasibility and alternative approaches to it. Nevertheless, the ethical underpinnings of the case for assisted colonization are claims about the value of species. A complete discussion of assisted colonization needs to include assessment of these claims. For each type of value that species are thought to possess it is necessary to determine whether it is plausible that species possess the type of value and, if so, to what extent their possessing it justifies assisted colonization. I conducted such an assessment for each of the predominant types of value ascribed to species: ecological, instrumental (including option value), existence, and intrinsic value (including interest‐based, objective, and valuer‐dependent intrinsic value). The vast majority of species, including several that have been proposed as candidates for assisted colonization, have much less value than is often presumed. Moreover, with respect to some types of value, assisted colonization would not fully preserve the value of the target species even if it were to keep the target species in existence. Therefore, the case for assisted colonization is significantly weaker and more qualified than its advocates often suppose. There may be exceptional species for which assisted colonization is well justified—and for this reason, case‐by‐case assessment is necessary—but in general the burden of justification generated by the ecological risks associated with assisted colonization is not met by the value potentially preserved by assisted colonization. This suggests that assisted colonization ought to have, at most, a very minor role in the portfolio of ecosystem management practices, even as it pertains to species conservation under conditions of rapid climate change.     

Preserving Population Allele Frequencies in Ex Situ Conservation Programs

Abstract: Optimization of contributions of parents to progeny by minimizing the average coancestry of the progeny is an effective strategy for maintaining genetic diversity in ex situ conservation programs, but its application on the basis of molecular markers has the negative collateral effect of homogenizing the allelic frequencies at each locus. Because one of the objectives of a conservation program is to preserve the genetic composition of the original endangered population, we devised a method in which markers are used to maintain the allele frequency distribution at each locus as closely as possible to that of the native population. Contributions of parents were obtained so as to minimize changes in allele frequency for a set of molecular markers in a population of reduced size. We used computer simulations, under a range of scenarios, to assess the effectiveness of the method in comparison with methods in which contributions of minimum coancestry are sought, either making use of molecular markers or genealogical information. Our simulations indicated that the proposed method effectively maintained the original distribution of allele frequencies, particularly under strong linkage, and maintained acceptable levels of genetic diversity in the population. Nevertheless, contributions of minimum coancestry determined from pedigree information but ignoring the genealogy previous to the conservation program, was the most effective method for maintaining allelic frequencies in realistic situations.     

Classification of Climate‐Change‐Induced Stresses on Biological Diversity

Abstract: Conservation actions need to account for and be adapted to address changes that will occur under global climate change. The identification of stresses on biological diversity (as defined in the Convention on Biological Diversity) is key in the process of adaptive conservation management. We considered any impact of climate change on biological diversity a stress because such an effect represents a change (negative or positive) in key ecological attributes of an ecosystem or parts of it. We applied a systemic approach and a hierarchical framework in a comprehensive classification of stresses to biological diversity that are caused directly by global climate change. Through analyses of 20 conservation sites in 7 countries and a review of the literature, we identified climate‐change‐induced stresses. We grouped the identified stresses according to 3 levels of biological diversity: stresses that affect individuals and populations, stresses that affect biological communities, and stresses that affect ecosystem structure and function. For each stress category, we differentiated 3 hierarchical levels of stress: stress class (thematic grouping with the coarsest resolution, 8); general stresses (thematic groups of specific stresses, 21); and specific stresses (most detailed definition of stresses, 90). We also compiled an overview of effects of climate change on ecosystem services using the categories of the Millennium Ecosystem Assessment and 2 additional categories. Our classification may be used to identify key climate‐change‐related stresses to biological diversity and may assist in the development of appropriate conservation strategies. The classification is in list format, but it accounts for relations among climate‐change‐induced stresses.     

Protection of Genetic Diversity and Maintenance of Connectivity among Reef Corals within Marine Protected Areas

Abstract: High‐latitude coral reefs (HLRs) are potentially vulnerable marine ecosystems facing well‐documented threats to tropical reefs and exposure to suboptimal temperatures and insolation. In addition, because of their geographic isolation, HLRs may have poor or erratic larval connections to tropical reefs and a reduced genetic diversity and capacity to respond to environmental change. On Australia's east coast, a system of marine protected areas (MPAs) has been established with the aim of conserving HLRs in part by providing sources of colonizing larvae. To examine the effectiveness of existing MPAs as networks for dispersal, we compared genetic diversity within and among the HLRs in MPAs and between these HLRs and tropical reefs on the southern Great Barrier Reef (GBR). The 2 coral species best represented on Australian HLRs (the brooding Pocillopora damicornis and the broadcast‐spawning Goniastrea australensis) exhibited sharply contrasting patterns of diversity and connectedness. For P. damicornis, the 8‐locus genetic and genotypic diversity declined dramatically with increasing latitude (N_a= 3.6–1.2, H_e= 0.3–0.03, N_g:N = 0.87–0.06), although population structure was consistent with recruitment derived largely from sexual reproduction (G_o:G_e= 1.28–0.55). Genetic differentiation was high among the HLRs (F_ST[SD]= 0.32 [0.08], p < 0.05) and between the GBR and the HLRs (F_ST= 0.24 [0.06], p < 0.05), which indicates these temperate populations are effectively closed. In contrast for G. australensis, 9‐locus genetic diversity was more consistent across reefs (N_a= 4.2–3.9, H_e= 0.3–0.26, N_g:N = 1–0.61), and there was no differentiation among regions (F_ST= 0.00 [0.004], p > 0.05), which implies the HLRs and the southern GBR are strongly interconnected. Our results demonstrate that although the current MPAs appear to capture most of the genetic diversity present within the HLR systems for these 2 species, their sharply contrasting patterns of connectivity indicate some taxa, such as P. damicornis, will be more vulnerable than others, and this disparity will provide challenges for future management.     

Joint Effects of Inbreeding and Local Adaptation on the Evolution of Genetic Load after Fragmentation

Abstract: Disruption of gene flow among demes after landscape fragmentation can facilitate local adaptation but increase the effect of genetic drift and inbreeding. The joint effects of these conflicting forces on the mean fitness of individuals in a population are unknown. Through simulations, we explored the effect of increased isolation on the evolution of genetic load over the short and long term when fitness depends in part on local adaptation. We ignored genetic effects on demography. We modeled complex genomes, where a subset of the loci were under divergent selection in different localities. When a fraction of the loci were under heterogeneous selection, isolation increased mean fitness in larger demes made up of hundreds of individuals because of improved local adaptation. In smaller demes of tens of individuals, increased isolation improved local adaptation very little and reduced overall fitness. Short‐term improvement of mean fitness after fragmentation may not be indicative of the long‐term evolution of fitness. Whatever the deme size and potential for local adaptation, migration of one or two individuals per generation minimized the genetic load in general. The slow dynamics of mean fitness following fragmentation suggests that conservation measures should be implemented before the consequences of isolation on the genetic load become of concern.     

How economics can further the success of ecological restoration

Restoration scientists and practitioners have recently begun to include economic and social aspects in the design and investment decisions for restoration projects. With few exceptions, ecological restoration studies that include economics focus solely on evaluating costs of restoration projects. However, economic principles, tools, and instruments can be applied to a range of other factors that affect project success. We considered the relevance of applying economics to address 4 key challenges of ecological restoration: assessing social and economic benefits, estimating overall costs, project prioritization and selection, and long‐term financing of restoration programs. We found it is uncommon to consider all types of benefits (such as nonmarket values) and costs (such as transaction costs) in restoration programs. Total benefit of a restoration project can be estimated using market prices and various nonmarket valuation techniques. Total cost of a project can be estimated using methods based on property or land‐sale prices, such as hedonic pricing method and organizational surveys. Securing continuous (or long‐term) funding is also vital to accomplishing restoration goals and can be achieved by establishing synergy with existing programs, public–private partnerships, and financing through taxation.     

Securing the Demographic and Genetic Future of Tuatara through Assisted Colonization

Abstract: Climate change poses a particular threat to species with fragmented distributions and little or no capacity to migrate. Assisted colonization, moving species into regions where they have not previously occurred, aims to establish populations where they are expected to survive as climatic envelopes shift. However, adaptation to the source environment may affect whether species successfully establish in new regions. Assisted colonization has spurred debate among conservation biologists and ecologists over whether the potential benefits to the threatened species outweigh the potential disruption to recipient communities. In our opinion, the debate has been distracted by controversial examples, rather than cases where assisted colonization may be a viable strategy. We present a strategic plan for the assisted migration of tuatara (Sphenodon punctatus), an endemic New Zealand reptile. The plan includes use of extant populations as reference points for comparisons with assisted‐colonization populations with respect to demography, phenotypic plasticity, and phenology; optimization of genetic variation; research to fill knowledge gaps; consideration of host and recipient communities; and inclusion of stakeholders in the planning stage. When strategically planned and monitored, assisted colonization could meet conservation and research goals and ultimately result in the establishment of long‐term sustainable populations capable of persisting during rapid changes in climate.     

Rank aggregation of local expert knowledge for conservation planning of the critically endangered saola

There has been much recent interest in using local knowledge and expert opinion for conservation planning, particularly for hard‐to‐detect species. Although it is possible to ask for direct estimation of quantities such as population size, relative abundance is easier to estimate. However, an expert's knowledge is often geographically restricted relative to the area of interest. Combining (or aggregating) experts’ assessments of relative abundance is difficult when each expert only knows a part of the area of interest. We used Google's PageRank algorithm to aggregate ranked abundance scores elicited from local experts through a rapid rural‐appraisal method. We applied this technique to conservation planning for the saola (Pseudoryx nghetinhensis), a poorly known bovid. Near a priority landscape for the species, composed of 3 contiguous protected areas, we asked groups of local people to indicate relative abundances of saola and other species by placing beans on community maps. For each village, we used this information to rank areas within the knowledge area of that village for saola abundance. We used simulations to compare alternative methods to aggregate the rankings from the different villages. The best‐performing method was then used to produce a single map of relative abundance across the entire landscape, an area larger than that known to any one village. This map has informed prioritization of surveys and conservation action in the continued absence of direct information about the saola.     

Estimating Extinction Risk with Metapopulation Models of Large‐Scale Fragmentation

Habitat loss is the principal threat to species. How much habitat remains—and how quickly it is shrinking—are implicitly included in the way the International Union for Conservation of Nature determines a species’ risk of extinction. Many endangered species have habitats that are also fragmented to different extents. Thus, ideally, fragmentation should be quantified in a standard way in risk assessments. Although mapping fragmentation from satellite imagery is easy, efficient techniques for relating maps of remaining habitat to extinction risk are few. Purely spatial metrics from landscape ecology are hard to interpret and do not address extinction directly. Spatially explicit metapopulation models link fragmentation to extinction risk, but standard models work only at small scales. Counterintuitively, these models predict that a species in a large, contiguous habitat will fare worse than one in 2 tiny patches. This occurs because although the species in the large, contiguous habitat has a low probability of extinction, recolonization cannot occur if there are no other patches to provide colonists for a rescue effect. For 4 ecologically comparable bird species of the North Central American highland forests, we devised metapopulation models with area‐weighted self‐colonization terms; this reflected repopulation of a patch from a remnant of individuals that survived an adverse event. Use of this term gives extra weight to a patch in its own rescue effect. Species assigned least risk status were comparable in long‐term extinction risk with those ranked as threatened. This finding suggests that fragmentation has had a substantial negative effect on them that is not accounted for in their Red List category. Estimación del Riesgo de Extinción Mediante Modelos Metapoblacionales de Fragmentación a Gran Escala