Exposing extinction risk analysis to pathogens: Is disease just another form of density dependence?

In the United States and several other countries., the development of population viability analyses (PVA) is a legal requirement of any species survival plan developed for threatened and endangered species. Despite the importance of pathogens in natural populations, little attention has been given to host-pathogen dynamics in PVA. To study the effect of infectious pathogens on extinction risk estimates generated from PVA, we review and synthesize the relevance of host-pathogen dynamics in analyses of extinction risk. We then develop a stochastic, density-dependent host-parasite model to investigate the effects of disease on the persistence of endangered populations. We show that this model converges on a Ricker model of density dependence under a suite of limiting assumptions, including. a high probability that epidemics will arrive and occur. Using this modeling framework, we then quantify: (1) dynamic differences between time series generated by disease and Ricker processes with the same parameters; (2) observed probabilities of quasi-extinction for populations exposed to disease or self-limitation; and (3) bias in probabilities of quasi-extinction estimated by density-independent PVAs when populations experience either form of density dependence. Our results suggest two generalities about the relationships among disease, PVA, and the management of endangered species. First, disease more strongly increases variability in host abundance and, thus, the probability of quasi-extinction, than does self-limitation. This result stems from the fact that the effects and the probability of occurrence of disease are both density dependent. Second, estimates of quasi-extinction are more often overly optimistic for populations experiencing disease than for those subject to self-limitation. Thus, although the results of density-independent PVAs may be relatively robust to some particular assumptions about density dependence, they are less robust when endangered populations are known to be susceptible to disease. If potential management actions involve manipulating pathogens, then it may be useful to. model disease explicitly.

The consistency of extinction risk classification protocols

Systematic protocols that use decision rules or scores arc, seen to improve consistency and transparency in classifying the conservation status of species. When applying these protocols, assessors are typically required to decide on estimates for attributes That are inherently uncertain, Input data and resulting classifications are usually treated as though they arc, exact and hence without operator error We investigated the impact of data interpretation on the consistency of protocols of extinction risk classifications and diagnosed causes of discrepancies when they occurred. We tested three widely used systematic classification protocols employed by the World Conservation Union, NatureServe, and the Florida Fish and Wildlife Conservation Commission. We provided 18 assessors with identical information for 13 different species to infer estimates for each of the required parameters for the three protocols. The threat classification of several of the species varied from low risk to high risk, depending on who did the assessment. This occurred across the three Protocols investigated. Assessors tended to agree on their placement of species in the highest (50-70%) and lowest risk categories (20-40%), but There was poor agreement on which species should be placed in the intermediate categories, Furthermore, the correspondence between The three classification methods was unpredictable, with large variation among assessors. These results highlight the importance of peer review and consensus among multiple assessors in species classifications and the need to be cautious with assessments carried out 4), a single assessor Greater consistency among assessors requires wide use of training manuals and formal methods for estimating parameters that allow uncertainties to be represented, carried through chains of calculations, and reported transparently.

Theory for designing nature reserves for single species

We examine the question of the optimal number of reserves that should be established to maximize the persistence of a species. We assume that the mean time to extinction of a single population increases as a power of the habitat area, that there is a certain amount of habitat to be reserved, and that the aim is to determine how this habitat is most efficiently divided. The optimal configuration depends on whether the management objective is to maximize the mean time to extinction or minimize the risk of extinction. When maximizing the mean time to extinction, the optimal number of independent reserves does not depend on the amount of available habitat for the reserve system. In contrast, the risk of extinction is minimized when individual reserves are equal to the optimal patch size, making the optimal number of reserves linearly proportional to the amount of available habitat. A model that includes dispersal and correlation in the incidence of extinction demonstrates the importance of considering the relative rate at which these two factors decrease with distance between reserves. A small number of reserves is optimal when the mean time to extinction increases rapidly with habitat area or when risks of extinction are high.

Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.

A new method for conservation planning for the persistence of multiple species

Although the aim of conservation planning is the persistence of biodiversity, current methods trade-off ecological realism at a species level in favour of including multiple species and landscape features. For conservation planning to be relevant, the impact of landscape configuration on population processes and the viability of species needs to be considered. We present a novel method for selecting reserve systems that maximize persistence across multiple species, subject to a conservation budget. We use a spatially explicit metapopulation model to estimate extinction risk, a function of the ecology of the species and the amount, quality and configuration of habitat. We compare our new method with more traditional, area-based reserve selection methods, using a ten-species case study, and find that the expected loss of species is reduced 20-fold. Unlike previous methods, we avoid designating arbitrary weightings between reserve size and configuration; rather, our method is based on population processes and is grounded in ecological theory.

Objectives for multiple-species conservation planning

The first step in conservation planning is to identify objectives. Most stated objectives for conservation, such as to maximize biodiversity outcomes, are too vague to be useful within a decision-making framework. One way to clarify the issue is to define objectives in terms of the risk of extinction for multiple species. Although the assessment of extinction risk for single species is common, few researchers have formulated an objective function that combines the extinction risks of multiple species. We sought to translate the broad goal of maximizing the viability of species into explicit objectives for use in a decision-theoretic approach to conservation planning. We formulated several objective functions based on extinction risk across many species and illustrated the differences between these objectives with simple examples. Each objective function was the mathematical representation of an approach to conservation and emphasized different levels of threat Our objectives included minimizing the joint probability of one or more extinctions, minimizing the expected number of extinctions, and minimizing the increase in risk of extinction from the best-case scenario. With objective functions based on joint probabilities of extinction across species, any correlations in extinction probabilities bad to be known or the resultant decisions were potentially misleading. Additive objectives, such as the expected number of extinctions, did not produce the same anomalies. We demonstrated that the choice of objective function is central to the decision-making process because alternative objective functions can lead to a different ranking of management options. Therefore, decision makers need to think carefully in selecting and defining their conservation goals.

Protocols for listing threatened species can forecast extinction

Risk-ranking protocols are used widely to classify the conservation status of the world's species. Here we report on the first empirical assessment of their reliability by using a retrospective study of 18 pairs of bird and mammal species (one species extinct and the other extant) with eight different assessors. The performance of individual assessors varied substantially, but performance was improved by incorporating uncertainty in parameter estimates and consensus among the assessors. When this was done, the ranks from the protocols were consistent with the extinction outcome in 70-80% of pairs and there were mismatches in only 10-20% of cases. This performance was similar to the subjective judgements of the assessors after they had estimated the range and population parameters required by the protocols, and better than any single parameter. When used to inform subjective judgement, the protocols therefore offer a means of reducing unpredictable biases that may be associated with expert input and have the advantage of making the logic behind assessments explicit. We conclude that the protocols are useful for forecasting extinctions, although they are prone to some errors that have implications for conservation. Some level of error is to be expected, however, given the influence of chance on extinction. The performance of risk assessment protocols may be improved by providing training in the application of the protocols, incorporating uncertainty in parameter estimates and using consensus among multiple assessors, including some who are experts in the application of the protocols. Continued testing and refinement of the protocols may help to provide better absolute estimates of risk, particularly by re-evaluating how the protocols accommodate missing data.