Toward an integrative molecular approach to wildlife disease

Pathogens pose serious threats to human health, agricultural investment, and biodiversity conservation through the emergence of zoonoses, spillover to domestic livestock, and epizootic outbreaks. As such, wildlife managers are often tasked with mitigating the negative effects of disease. Yet, parasites form a major component of biodiversity that often persist. This is due to logistical challenges of implementing management strategies and to insufficient understanding of host–parasite dynamics. We advocate for an inclusive understanding of molecular diversity in driving parasite infection and variable host disease states in wildlife systems. More specifically, we examine the roles of genetic, epigenetic, and commensal microbial variation in disease pathogenesis. These include mechanisms underlying parasite virulence and host resistance and tolerance, and the development, regulation, and parasite subversion of immune pathways, among other processes. Case studies of devil facial tumor disease in Tasmanian devils (Sarcophilus harrisii) and chytridiomycosis in globally distributed amphibians exemplify the broad range of questions that can be addressed by examining different facets of molecular diversity. For particularly complex systems, integrative molecular analyses present a promising frontier that can provide critical insights necessary to elucidate disease dynamics operating across scales. These insights enable more accurate risk assessment, reconstruction of transmission pathways, discernment of optimal intervention strategies, and development of more effective and ecologically sound treatments that minimize damage to the host population and environment. Such measures are crucial when mitigating threats posed by wildlife disease to humans, domestic animals, and species of conservation concern.     

Assessing species reintroduction sites based on future climate suitability for food resources

The reintroduction of a species that is extinct in the wild demands caution because reintroduction locations may be associated with threats, such as hunting, poor-quality habitat, and climate change. This is the case for Cyanopsitta spixii (Spix's Macaw), which has been extinct in the wild since 2000. The few living individuals were created in captivity and will be used in a reintroduction project within the species’ original distribution area, the Caatinga domain (Brazil). Because the occurrence records for this bird are old and inaccurate, we investigated the current and future environmental suitability of the 14 plant species used by C. spixii as resource. These plants are key elements for the long-term reestablishment of the species in the wild, so the use of models helps in the assessment of the effects of climate change on the availability of these resources for the species and informs selection of the best places for reintroduction. We based our models of environmental suitability on 19 bioclimatic variables and nine physical soil and topography variables. Climate projections were created for the present and for the year 2070 with an optimistic (SSP2-4.5) and a pessimistic (SSP5-8.5) climate scenario. Both future climate scenarios lead to a reduction in area of environmental suitability that overlapped for all the plant species: 33% reduction for SSP2-4.5 and 63% reduction for SSP5-8.5. If our projections materialize, climate change could thus affect the distribution of key resources, and the maintenance of C. spixii would depend on restoration of degraded areas, especially riparian forests, and the preservation of already existing natural areas. The Caatinga domain is very threatened by habitat loss and, for the success of this reintroduction project, the parties involved must act to protect the species and the resources it uses.     

Moving from trends to benchmarks by using regression tree analysis to find inbreeding thresholds in a critically endangered bird

Understanding how inbreeding affects endangered species in conservation breeding programs is essential for their recovery. The Hawaiian Crow (‘Alalā) (Corvus hawaiiensis) is one of the world's most endangered birds. It went extinct in the wild in 2002, and, until recent release efforts starting in 2016, nearly all of the population remained under human care for conservation breeding. Using pedigree inbreeding coefficients (F), we evaluated the effects of inbreeding on Hawaiian Crow offspring survival and reproductive success. We used regression tree analysis to identify the level of inbreeding (i.e., inbreeding threshold) that explains a substantial decrease in ‘Alalā offspring survival to recruitment. Similar to a previous study of inbreeding in ‘Alalā, we found that inbreeding had a negative impact on offspring survival but that parental (vs. artificial) egg incubation improved offspring survival to recruitment. Furthermore, we found that inbreeding did not substantially affect offspring reproductive success, based on the assumption that offspring that survive to adulthood breed with distantly related mates. Our novel application of regression tree analysis showed that offspring with inbreeding levels exceeding F = 0.098 were 69% less likely to survive to recruitment than more outbred offspring, providing a specific threshold value for ongoing population management. Our results emphasize the importance of assessing inbreeding depression across all life history stages, confirm the importance of prioritizing parental over artificial egg incubation in avian conservation breeding programs, and demonstrate the utility of regression tree analysis as a tool for identifying inbreeding thresholds, if present, in any pedigree-managed population.     

Examining the relationship between local extinction risk and position in range

Over half of globally threatened animal species have experienced rapid geographic range loss. Identifying the parts of species’ distributions most vulnerable to local extinction would benefit conservation planning. However, previous studies give little consensus on whether ranges decline to the core or edge. We built on previous work by using empirical data to examine the position of recent local extinctions within species’ geographic ranges, address range position as a continuum, and explore the influence of environmental factors. We aggregated point‐locality data for 125 Galliform species from across the Palearctic and Indo‐Malaya into equal‐area half‐degree grid cells and used a multispecies dynamic Bayesian occupancy model to estimate rates of local extinctions. Our model provides a novel approach to identify loss of populations from within species ranges. We investigated the relationship between extinction rates and distance from range edge by examining whether patterns were consistent across biogeographic realm and different categories of land use. In the Palearctic, local extinctions occurred closer to the range edge than range core in both unconverted and human‐dominated landscapes. In Indo‐Malaya, no pattern was found for unconverted landscapes, but in human‐dominated landscapes extinctions tended to occur closer to the core than the edge. Our results suggest that local and regional factors override general spatial patterns of recent local extinction within species’ ranges and highlight the difficulty of predicting the parts of a species’ distribution most vulnerable to threat.     

Sentiment analysis of the Twitter response to Netflix's Our Planet documentary

The role of nature documentaries in shaping public attitudes and behavior toward conservation and wildlife issues is unclear. We analyzed the emotional content of over 2 million tweets related to Our Planet, a major nature documentary released on Netflix, with dictionary and rule-based automatic sentiment analysis. We also compared the sentiment associated with species mentioned in Our Planet and a set of control species with similar features but not mentioned in the documentary. Tweets were largely negative in sentiment at the time of release of the series. This effect was primarily linked to the highly skewed distributions of retweets and, in particular, to a single negatively valenced and massively retweeted tweet (>150,000 retweets). Species mentioned in Our Planet were associated with more negative sentiment than the control species, and this effect coincided with a short period following the airing of the series. Our results are consistent with a general negativity bias in cultural transmission and document the difficulty of evoking positive sentiment, on social media and elsewhere, in response to environmental problems.     

Fundamental insights on when social network data are most critical for conservation planning

As declines in biodiversity accelerate, there is an urgent imperative to ensure that every dollar spent on conservation counts toward species protection. Systematic conservation planning is a widely used approach to achieve this, but there is growing concern that it must better integrate the human social dimensions of conservation to be effective. Yet, fundamental insights about when social data are most critical to inform conservation planning decisions are lacking. To address this problem, we derived novel principles to guide strategic investment in social network information for systematic conservation planning. We considered the common conservation problem of identifying which social actors, in a social network, to engage with to incentivize conservation behavior that maximizes the number of species protected. We used simulations of social networks and species distributed across network nodes to identify the optimal state-dependent strategies and the value of social network information. We did this for a range of motif network structures and species distributions and applied the approach to a small-scale fishery in Kenya. The value of social network information depended strongly on both the distribution of species and social network structure. When species distributions were highly nested (i.e., when species-poor sites are subsets of species-rich sites), the value of social network information was almost always low. This suggests that information on how species are distributed across a network is critical for determining whether to invest in collecting social network data. In contrast, the value of social network information was greatest when social networks were highly centralized. Results for the small-scale fishery were consistent with the simulations. Our results suggest that strategic collection of social network data should be prioritized when species distributions are un-nested and when social networks are likely to be centralized.     

Evaluating whether nature's intrinsic value is an axiom of or anathema to conservation

That at least some aspects of nature possess intrinsic value is considered by some an axiom of conservation. Others consider nature's intrinsic value superfluous or anathema. This range of views among mainstream conservation professionals potentially threatens the foundation of conservation. One challenge in resolving this disparity is that disparaging portrayals of nature's intrinsic value appear rooted in misconceptions and unfounded presumptions about what it means to acknowledge nature's intrinsic value. That acknowledgment has been characterized as vacuous, misanthropic, of little practical consequence to conservation, adequately accommodated by economic valuation, and not widely accepted in society. We reviewed the philosophical basis for nature's intrinsic value and the implications for acknowledging that value. Our analysis is rooted to the notion that when something possesses intrinsic value it deserves to be treated with respect for what it is, with concern for its welfare or in a just manner. From this basis, one can only conclude that nature's intrinsic value is not a vacuous concept or adequately accommodated by economic valuation. Acknowledging nature's intrinsic value is not misanthropic because concern for nature's welfare (aside from its influence on human welfare) does not in any way preclude also being concerned for human welfare. The practical import of acknowledging nature's intrinsic value rises from recognizing all the objects of conservation concern (e.g., many endangered species) that offer little benefit to human welfare. Sociological and cultural evidence indicates the belief that at least some elements of nature possess intrinsic value is widespread in society. Our reasoning suggests the appropriateness of rejecting the assertion that nature's intrinsic value is anathema to conservation and accepting its role as an axiom. Evaluar si el Valor Intrínseco de la Naturaleza es un Axioma o un Anatema para la Conservación     

Effects of Multiple Levels of Social Organization on Survival and Abundance

Abstract: Identifying how social organization shapes individual behavior, survival, and fecundity of animals that live in groups can inform conservation efforts and improve forecasts of population abundance, even when the mechanism responsible for group‐level differences is unknown. We constructed a hierarchical Bayesian model to quantify the relative variability in survival rates among different levels of social organization (matrilines and pods) of an endangered population of killer whales (Orcinus orca). Individual killer whales often participate in group activities such as prey sharing and cooperative hunting. The estimated age‐specific survival probabilities and survivorship curves differed considerably among pods and to a lesser extent among matrilines (within pods). Across all pods, males had lower life expectancy than females. Differences in survival between pods may be caused by a combination of factors that vary across the population's range, including reduced prey availability, contaminants in prey, and human activity. Our modeling approach could be applied to demographic rates for other species and for parameters other than survival, including reproduction, prey selection, movement, and detection probabilities.     

Interpreting beta‐diversity components over time to conserve metacommunities in highly dynamic ecosystems

The concept of metacommunity (i.e., a set of local communities linked by dispersal) has gained great popularity among community ecologists. However, metacommunity research mostly addresses questions on spatial patterns of biodiversity at the regional scale, whereas conservation planning requires quantifying temporal variation in those metacommunities and the contributions that individual (local) sites make to regional dynamics. We propose that recent advances in diversity‐partitioning methods may allow for a better understanding of metacommunity dynamics and the identification of keystone sites. We used time series of the 2 components of beta diversity (richness and replacement) and the contributions of local sites to these components to examine which sites controlled source‐sink dynamics in a highly dynamic model system (an intermittent river). The relative importance of the richness and replacement components of beta diversity fluctuated over time, and sample aggregation led to underestimation of beta diversity by up to 35%. Our literature review revealed that research on intermittent rivers would benefit greatly from examination of beta‐diversity components over time. Adequately appraising spatiotemporal variability in community composition and identifying sites that are pivotal for maintaining biodiversity at the landscape scale are key needs for conservation prioritization and planning. Thus, our framework may be used to guide conservation actions in highly dynamic ecosystems when time‐series data describing biodiversity across sites connected by dispersal are available.     

Creation of a Gilded Trap by the High Economic Value of the Maine Lobster Fishery

Abstract: Unsustainable fishing simplifies food chains and, as with aquaculture, can result in reliance on a few economically valuable species. This lack of diversity may increase risks of ecological and economic disruptions. Centuries of intense fishing have extirpated most apex predators in the Gulf of Maine (United States and Canada), effectively creating an American lobster (Homarus americanus) monoculture. Over the past 20 years, the economic diversity of marine resources harvested in Maine has declined by almost 70%. Today, over 80% of the value of Maine's fish and seafood landings is from highly abundant lobsters. Inflation‐corrected income from lobsters in Maine has steadily increased by nearly 400% since 1985. Fisheries managers, policy makers, and fishers view this as a success. However, such lucrative monocultures increase the social and ecological consequences of future declines in lobsters. In southern New England, disease and stresses related to increases in ocean temperature resulted in more than a 70% decline in lobster abundance, prompting managers to propose closing that fishery. A similar collapse in Maine could fundamentally disrupt the social and economic foundation of its coast. We suggest the current success of Maine's lobster fishery is a gilded trap. Gilded traps are a type of social trap in which collective actions resulting from economically attractive opportunities outweigh concerns over associated social and ecological risks or consequences. Large financial gain creates a strong reinforcing feedback that deepens the trap. Avoiding or escaping gilded traps requires managing for increased biological and economic diversity. This is difficult to do prior to a crisis while financial incentives for maintaining the status quo are large. The long‐term challenge is to shift fisheries management away from single species toward integrated social‐ecological approaches that diversify local ecosystems, societies, and economies.