Population Viability Analysis of the Florida Manatee (Trichechus manatus latirostris), 1976–1991

Recent development of age-determination techniques for Florida manatees (Trichechus manatus latirostris) has permitted derivation of age-specific data on reproduction and survival of a sample of 1212 carcasses obtained throughout Florida from 1976–1991. Population viability analysis using these data projects a slightly negative growth rate (−0.003) and an unacceptably low probability of persistence (0.44) over 1000 years. The main factors affecting population projections were adult survival and fecundity. A 10% increase in adult mortality would drive the population to extinction over a 1000-year time scale, whereas a 10% decrease in adult mortality would allow slow population growth. A 10% decrease in reproduction would also result in extinction. We conclude that management must focus on retaining and improving the conditions under which manatee demography operates. The major identified agent of mortality is boat-manatee collisions, and rapidly increasing numbers of humans and registered boats portend an increase in manatee mortality. Zoning of manatee-occupied waters for reductions in boating activity and speed is essential to safeguard the manatee population. If boating regulations being implemented by the state of Florida in each of 13 key coastal counties are completed, enforced, and effective, manatees and human recreation could coexist indefinitely. If regulation is unsuccessful, the Florida manatee population is likely to decline slowly toward extinction.     

The Interplay between Climate Variability and Density Dependence in the Population Viability of Chinook Salmon

Abstract:  The viability of populations is influenced by driving forces such as density dependence and climate variability, but most population viability analyses (PVAs) ignore these factors because of data limitations. Additionally, simplified PVAs produce limited measures of population viability such as annual population growth rate (λ) or extinction risk. Here we developed a "mechanistic" PVA of threatened Chinook salmon ( Oncorhynchus tshawytscha ) in which, based on 40 years of detailed data, we related freshwater recruitment of juveniles to density of spawners, and third-year survival in the ocean to monthly indices of broad-scale ocean and climate conditions. Including climate variability in the model produced important effects: estimated population viability was very sensitive to assumptions of future climate conditions and the autocorrelation contained in the climate signal increased mean population abundance while increasing probability of quasi extinction. Because of the presence of density dependence in the model, however, we could not distinguish among alternative climate scenarios through mean λ values, emphasizing the importance of considering multiple measures to elucidate population viability. Our sensitivity analyses demonstrated that the importance of particular parameters varied across models and depended on which viability measure was the response variable. The density-dependent parameter associated with freshwater recruitment was consistently the most important, regardless of viability measure, suggesting that increasing juvenile carrying capacity is important for recovery.     

Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography

Despite extensive study of pollination and plant reproduction on the one hand, and of plant demography on the other, we know remarkably little about links between seed production in successive generations, and hence about long-term population consequences of variation in pollination success. We bridged this "generation gap" in Ipomopsis aggregata, a long-lived semelparous wildflower that is pollinator limited, by adding varying densities of seeds to natural populations and following resulting plants through their entire life histories. To determine whether pollen limitation of seed production constrains rate of population growth in this species, we sowed seeds into replicated plots at a density that mimics typical pollination success and spacing of flowering plants in nature, and at twice that density to mimic full pollination. Per capita offspring survival, flower production, and contribution to population increase (lambda) did not decline with sowing density in this experiment, suggesting that typical I. aggregata populations freed from pollen limitation will grow over the short term. In a second experiment we addressed whether density dependence would eventually erase the growth benefits of full pollination, by sowing a 10-fold range of seed densities that falls within extremes estimated for the natural "seed rain" that reaches the soil surface. Per capita survival to flowering and age at flowering were again unaffected by sowing density, but offspring size, per capita flower production, and lambda declined with density. Such density dependence complicates efforts to predict population dynamics over the longer term, because it changes components of the life history (in this case fecundity) as a population grows. A complete understanding of how constraints on seed production affect long-term population growth will hinge on following offspring fates at least through flowering of the first offspring generation, and doing so for a realistic range of population densities.     

Climate correlates of 20 years of trophic changes in a high-elevation riparian system

The consequences of climate change for ecosystem structure and function remain largely unknown. Here, I examine the ability of climate variation to explain long-term changes in bird and plant populations, as well as trophic interactions in a high-elevation riparian system in central Arizona, USA, based on 20 years of study. Abundances of dominant deciduous trees have declined dramatically over the 20 years, correlated with a decline in overwinter snowfall. Snowfall can affect overwinter presence of elk, whose browsing can significantly impact deciduous tree abundance. Thus, climate may affect the plant community indirectly through effects on herbivores, but may also act directly by influencing water availability for plants. Seven species of birds were found to initiate earlier breeding associated with an increase in spring temperature across years. The advance in breeding time did not affect starvation of young or clutch size. Earlier breeding also did not increase the length of the breeding season for single-brooded species, but did for multi-brooded species. Yet, none of these phenology-related changes was associated with bird population trends. Climate had much larger consequences for these seven bird species by affecting trophic levels below (plants) and above (predators) the birds. In particular, the climate-related declines in deciduous vegetation led to decreased abundance of preferred bird habitat and increased nest predation rates. In addition, summer precipitation declined over time, and drier summers also were further associated with greater nest predation in all species. The net result was local extinction and severe population declines in some previously common bird species, whereas one species increased strongly in abundance, and two species did not show clear population changes. These data indicate that climate can alter ecosystem structure and function through complex pathways that include direct and indirect effects on abundances and interactions of multiple trophic components.     

Taxonomic and Geographic Patterns of Decline for Threatened and Endangered Species in the United States

Abstract: Species listed under the U.S. Endangered Species Act (i.e., listed species) have declined to the point that the probability of their extinction is high. The decline of these species, however, may manifest itself in different ways, including reductions in geographic range, number of populations, or overall abundance. Understanding the pattern of decline can help managers assess extinction probability and define recovery objectives. Although quantitative data on changes in geographic range, number of populations, and abundance usually do not exist for listed species, more often qualitative data can be obtained. We used qualitative data in recovery plans for federally listed species to determine whether each listed species declined in range size, number of populations, or abundance relative to historical levels. We calculated the proportion of listed species in each state (or equivalent) that declined in each of those ways. Nearly all listed species declined in abundance, and range size or number of populations declined in approximately 80% of species for which those data were available. Patterns of decline, however, differed taxonomically and geographically. Declines in range were more common among vertebrates than plants, whereas population extirpations were more common among plants. Invertebrates had high incidence of range and population declines. Narrowly distributed plants and invertebrates may be subject to acute threats that may result in population extirpations, whereas vertebrates may be affected by chronic threats that reduce the extent and size of populations. Additionally, in the eastern United States and U.S. coastal areas, where the level of land conversion is high, a greater percentage of species’ ranges declined and more populations were extirpated than in other areas. Species in the Southwest, especially plants, had fewer range and population declines than other areas. Such relations may help in the selection of species’ recovery criteria.     

Population Viability Analysis for an Endangered Plant

Abstract: Demographic modeling is used to understand the population viability of Furbish's lousewort, Pedicularis furbishiae , a perennial plant species endemic to the St. John River Valley in northern Maine. Environment-specific summaries of demographic parameters (survivorship, growth, and fecundity) over four years, organized into stage-based projection matrices, provide predictions of future population dynamics given a deterministic extension of past conditions. Stochastic modeling, using (I) empirically observed variation in demographic parameters, and (2) estimated rates of natural catastrophes, leads to predictions of extinction probability.
P. furbishiae viability has varied widely over the study period Viable populations with finite rates of increase > 1 are found where cover is low, woody plants do not dominate, and disturbance does not occur. Rates of increase vary over time, suggesting that stochastic analyses would be realistic. Stochastic measures of population viability incorporating environmental variation suggest that early successional environments, especially wetter sites, can support viable populations in the absence of disturbance. However; observed rates of natural catastrophe dominate viability estimates of individual populations. Metapopulation dynamics feature extinction rates that are greater than recolonization rates, and may be affected by land use in the watershed Species management needs to consider a large-scale view of the riverine corridor.     

Longevity can buffer plant and animal populations against changing climatic variability

Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.     

Effects of Social Structure and Prey Dynamics on Extinction Risk in Gray Wolves

Extinction models based on diffusion theory generally fail to incorporate two important aspects of population biology—social structure and prey dynamics. We include these aspects in an individual-based extinction model for small, isolated populations of the gray wolf (Canis lupus). Our model predicts mean times to extinction significantly longer than those predicted by more general (diffusion) models. According to our model, an isolated population of 50 wolves has a 95% chance of surviving just 9 years and only a 30% chance of surviving beyond 100 years. Reflecting the influence of social structure, a wolf population initially comprising 50 individuals is expected to persist only a few years longer, on average (71 years), than is a population initially comprising just a single reproductive pair (62 years). In contrast, substantially greater average prey abundance leads to dramatically longer expected persistence times. Autocorrelated prey dynamics result in a more complex distribution of extinction times than predicted by many extinction models. We contend that demographic stochasticity may pose the greatest threat to small, isolated wolf populations, although environmental stochasticity and genetic effects may compound this threat. Our work highlights the importance of considering social structure and resource dynamics in the development of population viability analyses.     

Extinction Dynamics in the American Marten (Martes americana)

We constructed a model of marten population dynamics and used it to investigate extinction processes across a wide range of parameter values. The model was based on rules governing the behavior and physiology of individual martens and focused on energy balance. Spatial dynamics and demographic and environmental stochasticity were incorporated. The outcome was the probability of extinction and quasiextinction (20 females remaining) over 500 years. Three qualitative forms of extinction were delineated. The first was deterministic extinction, associated with those parameter combinations leading to a negative population growth rate. The second was probabilistic extinction in systems with a strong positive growth rate but restricted population size due to habitat constraint. The transition from 100% persistence to 100% quasiextinction, as the input habitat size was decreased, was abrupt. The final form of extinction was in systems with a growth rate of approximately zero. Prey availability maintained an upper limit on these populations, but otherwise fluctuations in population size were essentially random, leading to nontrivial probabilities of extinction in even relatively large populations. A number of issues requiring further empirical research were identified. These included the relationship between habitat quality and marten reproduction, dispersal patterns and dispersal mortality, the effect of habitat edge on marten reproduction and mortality, and the characterization of the severity and frequency of catastrophic mortality as experienced by marten populations.     

Foliar damage to parental plants interacts to influence mating success of Ipomoea purpurea

Studies of how herbivory affects plant fitness often determine whether damage to one parent alters reproductive output (i.e., seed set or paternity) but ignore the possibility that the outcome may be different if both parents were damaged (i.e., the presence of maternal x paternal damage interactions). Using inbred lines of the common morning glory, Ipomoea purpurea, I conducted a series of greenhouse experiments to test whether foliar damage from a generalist insect herbivore, Trichoplusia ni, alters male and female fitness components when neither parent, one parent, or both I. purpurea parents had been damaged. In a single-donor experiment, flowers on both damaged and undamaged maternal plants received pollen from either damaged or undamaged paternal plants. I. purpurea flowers were more likely to be aborted when they received pollen from damaged paternal plants, or when maternal plants were both damaged and grown under low-resource conditions. Foliar damaged plants also produced less seed and pollen than undamaged plants, although seed mass and pollen viability were not affected by damage. In a multiple-donor experiment, flowers on damaged and undamaged maternal plants simultaneously received pollen from damaged and undamaged paternal plants, and F1 seeds were analyzed for paternity. Damaged paternal plants had reduced siring success compared to undamaged paternal plants, and this discrepancy was most pronounced when competition occurred on damaged maternal plants. Thus, damaged maternal plants were more "selective" than undamaged maternal plants. Although previous studies have demonstrated that herbivory can alter fruit and seed production and paternity patterns, this is the first study to show that the magnitude of herbivore damage experienced by both parents can interact to influence maternal and paternal mating success.     

Natural Die-Offs of Large Mammals: Implications for Conservation

The viability of populations is a central concern of biological conservation. The occurrence of catastrophic die-offs may greatly reduce the long-term viability of populations. Theoretical extinction models and viability analyses require information on the frequency of die-offs and on the distribution of die-off severities. A review of literature identified 96 natural die-offs in large mammal populations, with a die-off being defined as a peak-to-trough decline in estimated population numbers of at least 25%. If such die-offs are common, population viability analyses that ignore them may be overly optimistic. The severities of the natural die-offs of large mammals presented here are not uniformly distributed. There is a relative overabundance of die-offs in the 70–90% range, and an underabundance of die-offs greater than 90%. This may indicate the presence of buffers against population extinction. The reported causes of large mammal die-offs were significantly related to trophic level: herbivore die-offs were more often attributed to starvation, while carnivore die-offs were more often attributed to disease. Populations subject to large-scale phenomena such as drought and severe winters may not be protected from die-offs by population subdivision. On the other hand, populations subject to catastrophic disease epidemics may be protected by subdivision, and threatened by corridors between conservation areas and by translocation efforts.     

The Impact of Increased Environmental Stochasticity Due to Climate Change on the Dynamics of Asiatic Wild Ass

Abstract:  Theory proposes that increased environmental stochasticity negatively impacts population viability. Thus, in addition to the directional changes predicted for weather parameters under global climate change (GCC), the increase in variance of these parameters may also have a negative effect on biodiversity. As a case study, we assessed the impact of interannual variance in precipitation on the viability of an Asiatic wild ass ( Equus hemionus ) population reintroduced in Makhtesh Ramon Nature Reserve, Israel. We monitored the population from 1985 to 1999 to determine what environmental factors affect reproductive success. Annual precipitation during the year before conception, drought conditions during gestation, and population size determined reproductive success. We used the parameters derived from this model to assess population performance under various scenarios in a Leslie matrix type model with demographic and environmental stochasticity. Specifically, we used a change in the precipitation regime in our study area to formulate a GCC scenario and compared the simulated dynamics of the population with a no-change scenario. The coefficient of variation in population size under the global change scenario was 30% higher than under the no-change scenario. Minor die-offs (≥15%) following droughts increased extinction probability nearly 10-fold. Our results support the idea that an increase in environmental stochasticity due to GCC may, in itself, pose a significant threat to biodiversity.     

New Approaches Toward a Better Understanding of the Decline of Takahe (Porphyrio mantelli) in New Zealand

Island populations of endemic birds are known to be particularly susceptible to extinction. This paper focuses on factors behind past and present declines of the highly endangered Takahe ( Porphyrio mantelli ), a flightless rail endemic to New Zealand. Subfossil evidence indicates that Takahe were once found throughout this island nation, being most abundant along forest margins and streams in lowland regions. Their numbers have declined dramatically since human colonization about 800–1000 years ago, probably due to a combination of habitat destruction and hunting by early Polynesian settlers. Today, the wild Takahe population consists of about 100 adult birds in an isolated alpine habitat and approximately 30 individuals recently released on several small offshore islands. Despite protection and intensive management, including removal of an introduced competitor (red deer, Cervus elaphus ), the alpine population has continued to decline. In contrast, the Takahe's nearest relative, the Pukeko ( Porphyrio porphyrio ) has expanded its range across New Zealand despite heavy hunting pressure since its colonization from Australia less than 1000 years ago. We suggest that, unlike Pukeko, Takahe lack appropriate behavioral responses to cope with mammalian predators such as stoats ( Mustela erminea ), which have been introduced relatively recently by European colonists. A study comparing predator defense behavior between these two closely related species is currently underway.     

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.     

Genomic erosion in a demographically recovered bird species during conservation rescue

The pink pigeon (Nesoenas mayeri) is an endemic species of Mauritius that has made a remarkable recovery after a severe population bottleneck in the 1970s to early 1990s. Prior to this bottleneck, an ex situ population was established from which captive-bred individuals were released into free-living subpopulations to increase population size and genetic variation. This conservation rescue led to rapid population recovery to 400–480 individuals, and the species was twice downlisted on the International Union for the Conservation of Nature (IUCN) Red List. We analyzed the impacts of the bottleneck and genetic rescue on neutral genetic variation during and after population recovery (1993–2008) with restriction site-associated sequencing, microsatellite analyses, and quantitative genetic analysis of studbook data of 1112 birds from zoos in Europe and the United States. We used computer simulations to study the predicted changes in genetic variation and population viability from the past into the future. Genetic variation declined rapidly, despite the population rebound, and the effective population size was approximately an order of magnitude smaller than census size. The species carried a high genetic load of circa 15 lethal equivalents for longevity. Our computer simulations predicted continued inbreeding will likely result in increased expression of deleterious mutations (i.e., a high realized load) and severe inbreeding depression. Without continued conservation actions, it is likely that the pink pigeon will go extinct in the wild within 100 years. Conservation rescue of the pink pigeon has been instrumental in the recovery of the free-living population. However, further genetic rescue with captive-bred birds from zoos is required to recover lost variation, reduce expression of harmful deleterious variation, and prevent extinction. The use of genomics and modeling data can inform IUCN assessments of the viability and extinction risk of species, and it helps in assessments of the conservation dependency of populations.     

Directions in Conservation Biology: Comments on Caughley

The recent review by Caughley (1994) on approaches used in conservation biology suggested that there are two: the small population paradigm and the declining population paradigm. We believe that this division is overly simplistic and that it should not be perpetuated. Both the deterministic factors that reduce population size and the stochastic factors that lead to the final extinction of a small population are critical to consider in preventing extinction. Only through an overall and comprehensive effort, which we call inclusive population viability analysis, can extinction processes be understood and mitigated. In this context we discuss Caughley's comments about genetics, demography, and general population viability, with particular attention to cheetahs (Acinonyx jubatus) and Pacific salmon (Oncorhynchus sp. ) .     

Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant

Mutualisms are well known to influence individual fitness and the population dynamics of partner species, but little is known about whether they influence species distributions and the location of geographic range limits. Here, we examine the contribution of plant-pollinator interactions to the geographic range limit of the California endemic plant Clarkia xantiana ssp. xantiana. We show that pollinator availability declined from the center to the margin of the geographic range consistently across four years of study. This decline in pollinator availability was caused to a greater extent by variation in the abundance of generalist rather than specialist bee pollinators. Climate data suggest that patterns of precipitation in the current and previous year drove variation in bee abundance because of its effects on cues for bee emergence in the current year and the abundance of floral resources in the previous year. Experimental floral manipulations showed that marginal populations had greater outcross pollen limitation of reproduction, in parallel with the decline in pollinator abundance. Although plants are self-compatible, we found no evidence that autonomous selfing contributes to reproduction, and thus no evidence that it alleviates outcross pollen limitation in marginal populations. Furthermore, we found no association between the distance to the range edge and selfing rate, as estimated from sequence and microsatellite variation, indicating that the mating system has not evolved in response to the pollination environment at the range periphery. Overall, our results suggest that dependence on pollinators for reproduction may be an important constraint limiting range expansion in this system.     

Floater mortality within settlement areas can explain the Allee effect in breeding populations

The Allee effect (the positive relationship between population growth rate and population size) is a constraint of some animal populations at low numbers, which increases their likelihood of extinction because of a decrease in reproduction and/or survival. We were able to demonstrate that the Allee effect can be the result of a mortality increase affecting floaters (i.e. dispersing individuals able to enter as breeders in the reproductive population when a breeding territory or a potential mate – owner of a suitable breeding territory – becomes available). Previously, potential mechanisms underlying Allee effects were always related to the breeding portion of a population only. In contrast, our understanding of or solutions to population declines due to the Allee effects can reside elsewhere, away from breeding territories.     

A Behaviorally Explicit Demographic Model Integrating Habitat Selection and Population Dynamics in California Sea Lions

Abstract: Although there has been a call for the integration of behavioral ecology and conservation biology, there are few tools currently available to achieve this integration. Explicitly including information about behavioral strategies in population viability analyses may enhance the ability of conservation biologists to understand and estimate patterns of extinction risk. Nevertheless, most behavioral‐based PVA approaches require detailed individual‐based data that are rarely available for imperiled species. We present a mechanistic approach that incorporates spatial and demographic consequences of behavioral strategies into population models used for conservation. We developed a stage‐structured matrix model that includes the costs and benefits of movement associated with 2 habitat‐selection strategies (philopatry and direct assessment). Using a life table for California sea lions (Zalophus californianus), we explored the sensitivity of model predictions to the inclusion of these behavioral parameters. Including behavioral information dramatically changed predicted population sizes, model dynamics, and the expected distribution of individuals among sites. Estimated population sizes projected in 100 years diverged up to 1 order of magnitude among scenarios that assumed different movement behavior. Scenarios also exhibited different model dynamics that ranged from stable equilibria to cycles or extinction. These results suggest that inclusion of behavioral data in viability models may improve estimates of extinction risk for imperiled species. Our approach provides a simple method for incorporating spatial and demographic consequences of behavioral strategies into population models and may be easily extended to other species and behaviors to understand the mechanisms of population dynamics for imperiled populations.     

The Role of Behavior in Recent Avian Extinctions and Endangerments

Abstract: Understanding patterns of differential extinction and predicting the relative risks of extinction among extant species are among the most important problems in conservation biology. Although recent studies reveal that behavior can be a critical component in many species' extinctions or endangerments, current approaches to the problem of predicting extinction patterns largely ignore behavior. I reviewed how behavior can affect population persistence and then used recent avian extinctions and endangerments to illustrate behaviors relevant to extinction risk. Behaviors that affect population persistence can be grouped as aggregation, interspecific responses, dispersal, habitat selection, intraspecific behavior, and maladaptive behavior. Behavior that can affect extinction risk is not limited to birds; for example, in many taxonomic groups (vertebrate and invertebrate) there is evidence of socially facilitated reproduction in colonial species, Allee effects on reproductive success and survival, behavioral regulation of population size, and conspecific attraction to breeding sites. Incorporating specific behaviors into models predicting extinction probabilities and patterns should improve their predictions.