Phylogenetics support an ancient common origin of two scientific icons: Devils Hole and Devils Hole pupfish

The Devils Hole pupfish (Cyprinodon diabolis; DHP) is an icon of conservation biology. Isolated in a 50 m² pool (Devils Hole), DHP is one of the rarest vertebrate species known and an evolutionary anomaly, having survived in complete isolation for thousands of years. However, recent findings suggest DHP might be younger than commonly thought, potentially introduced to Devils Hole by humans in the past thousand years. As a result, the significance of DHP from an evolutionary and conservation perspective has been questioned. Here we present a high‐resolution genomic analysis of DHP and two closely related species, with the goal of thoroughly examining the temporal divergence of DHP. To this end, we inferred the evolutionary history of DHP from multiple random genomic subsets and evaluated four historical scenarios using the multispecies coalescent. Our results provide substantial information regarding the evolutionary history of DHP. Genomic patterns of secondary contact present strong evidence that DHP were isolated in Devils Hole prior to 20–10 ka and the model best supported by geological history and known mutation rates predicts DHP diverged around 60 ka, approximately the same time Devils Hole opened to the surface. We make the novel prediction that DHP colonized and have survived in Devils Hole since the cavern opened, and the two events (colonization and collapse of the cavern's roof) were caused by a common geologic event. Our results emphasize the power of evolutionary theory as a predictive framework and reaffirm DHP as an important evolutionary novelty, worthy of continued conservation and exploration.     

Population dynamics of the Devils Hole pupfish

Synopsis A model is constructed to simulate fluctuations in monthly population sizes of the Devils Hole pupfish between January 1973 and August 1976. A variety of biological parameters is estimated, and adult mortality is partitioned into natural and environmentally-dependent components. The simulations capture the seasonal fluctuations in population size, and only seven predicted population sizes differ from those observed by 20% or more. The model is used to make testable predictions about the life history of this species and interactions of the parameters are discussed.     

Evaluation of the role of refugia in conservation efforts for the Devils Hole pupfish,Cyprinodon diabolis Wales

The Hoover Dam Refugium was built to help insure the survival of the Devils Hole pupfish during an especially critical period. It served that purpose well. The Amargosa Pupfish Station added an additional, nearly identical artificial habitat to use in conservation and management of the Devils Hole pupfish. Contemporary concerns of conservation biology suggest that: 1) Genetic diversity or homogeneity of refugium populations should, when possible, be established by biochemical and morphological techniques; 2) protection of the natural habitat has been effected, and population levels have returned essentially to normal, therefore, management intervention in the natural population is not now appropriate; 3) refugium populations represent a unique opportunity to develop information useful in conservation and management of small populations of endangered fishes, if legal restrictions to such investigations can be accommodated; and 4) refugia, dependent on human activities for construction and maintenance, are less reliable than natural habitats.     

Maintained effects of fire on individual growth and survival rates in a spur-thighed tortoise population

Fires strongly influence the ecology of reptiles and have both direct and indirect effects on population dynamics as they affect life history traits. Here, we examine the effects of fire on individual growth patterns and on the survival rates of a tortoise Testudo graeca population in south-eastern Spain. We compare the biometric data from recaptures 4 years before and after a fire which burned 31 % of our study area. The von Bertalanffy and Gompertz growth models best describe the individual growth patterns for males and females. In males, but not females, fire significantly decreased the time required to reach their asymptotic size (k parameter). However, adult survival analyses reveal that the local survival rates lowered for both sexes after fire. Our work evidences that the effects of fire can be complex and maintained over time, affecting different life history traits.     

Adélie penguin (Pygoscelis adeliae) survival rates and their relationship to environmental indices in the South Shetland Islands,Antarctica

Seabird life history is typified by low fecundity, high adult survival rates, and relatively long lives. Such traits act as buffers, enabling persistence of populations under variable environmental conditions. Numerous studies, however, have suggested strong sensitivity of seabirds to environmental variability. In the Antarctic Peninsula region, for example, Adélie penguin (Pygoscelis adeliae) populations have declined during the last three decades, attributed largely to rapid changes in environmental conditions and food availability. We use 30 years of mark-recapture data from known-age individuals in the South Shetland Islands and capture-mark-recapture models to estimate survival rates with respect to such environmental variation. We investigated specifically whether negative trends in survival rates were evident and whether indices of global, regional, and local environmental conditions considered important for Adélie penguin survival explained the variability in survival rates. Overall, negative trends in juvenile survival were evident, but adult survival rates exhibited high interannual variability. Indices of sea ice extent had the strongest correlations with survival rates, particularly Weddell Sea ice extent during spring among adults (r = 0.62) and during winter for juveniles (r = 0.46). An analysis of deviance, however, suggested that single environmental covariates explained <30 % of the observed variation in the full mark-recapture models. Despite positive effects of sea ice extent on survival rates of Adélie penguins, limited explanatory power of several environmental conditions previously identified as important for Adélie penguin survival underscores the difficulty of predicting future population responses in this region of rapid environmental change.     

Birth-year and current-year influences on survival and recruitment rates of female Weddell seals

In long-lived species, juvenile survival typically is lower and more variable than adult survival, and modeling such variation is important for understanding population dynamics. Variability in juvenile survival can be related to birth- or current-year influences, and the birth-year influences can be transient, persistent, or intermediate in duration. We used multi-state models and data collected from 5,459 known-aged prebreeder female Weddell seals (Leptonychotes weddellii Lesson) tagged in Erebus Bay, Antarctica from 1980–2007 to evaluate the duration of potential birth-year influences on survival rates and the importance of birth- and current-year influences on survival and recruitment rates. Survival rates differed for each birth cohort and were positively related to current-year winter sea-ice conditions. The estimated duration of birth-cohort effects on survival was intermediate (6 years) rather than transient (2 years) or permanent. Estimated survivorship from birth to 6 years of age varied among cohorts from 0.13 (SE = 0.04) to 0.42 (SE = 0.06), and averaged 0.25 (SE = 0.02). Recruitment rates (probability of transitioning from prebreeder to breeder state) varied annually but apparently were not related to birth-year conditions. Our results provide evidence that birth- and current-year conditions act in combination to influence survival. Although for many long-lived species the influences of either birth- or current-year conditions on survival are well-studied, we suggest that modeling survival rates as a function of birth- and current-year influences simultaneously could lead to better understanding of survival and improved stochastic models to project population dynamics.     

Contrasting age-specific recruitment and survival at different spatial scales: a case study with the European storm petrel

Evolutionary studies on optimal decisions or conservation guidelines are often derived by generalising patterns from a single population, while inter‐population variability in life‐history traits is seldom considered. We investigated here how survival and recruitment probabilities changed with age at different geographical scales using the encounter histories of 5523 European storm petrels from three Mediterranean colonies, and also how our estimates of these parameters might be expected to affect population growth rates using population matrix models. We recorded similar patterns among colonies, but also important biological differences. Local survival, recruitment and breeding success increased with age at all colonies; the most distant of three colonies (Marettimo Is.) showed the largest differences. Strikingly, differences in recruitment were also found between two adjacent colonies (two caves from Benidorm Is.). Birds marked as adults from Marettimo and Benidorm colonies had a different survival, whereas we found no differences within Benidorm. Differences in survival were no longer apparent between the two islands at the end of the study following a reduction in predation by specialist gulls at Benidorm. Since birds marked as fledglings mostly recruited near the end of the study, their overall survival was high and in turn similar among colonies. Results from our population matrix models suggested that different age‐dependent patterns of demographic parameters can lead to similar population growth rates. Variability appeared to be greater for recruitment and the most sensitive parameter was adult survival. Thus conservation actions targeting this vulnerable species should focus on factors influencing adult survival. Differences in survival and recruitment among colonies could reflect the spatial heterogeneity in mortality due to predation and colony‐specific density dependent processes. Results highlight the importance of taking into account the potential spatio‐temporal heterogeneity among populations in vital rates, even in those traits that life‐history theory considers less important in driving population dynamics.     

Survival and population persistence in the critically endangered Tuamotu kingfisher

A wide range of threats affect populations of Pacific island birds and conservationists have been challenged to identify factors upon which to focus management. The Tuamotu kingfisher (Todiramphus gambieri) is one of the most endangered vertebrate species in the world, yet little has been published about basic biology or causes of the population decline. We used 4 years of mark-resight and territory resource information to model survival in juvenile and adult Tuamotu kingfishers. Annual survival of adult males (ϕ = 0.77) was similar to congeneric species, whereas survival of adult females (ϕ = 0.40) and juveniles (ϕ = 0.12) was much lower. The best-supported survival model indicated adult female survival was positively related to territory size, whereas adult male survival was negatively related to atoll forest within territories. We used parameter estimates from survival models in a life-stage simulation analysis to evaluate the relative influence of vital rates and territory habitats on population processes. Results indicated that adult female and juvenile survival had the greatest impact on Tuamotu kingfisher populations, accounting for 58% and 32% of variation in the finite rate of population increase, respectively. Nocturnal predation by rats (Rattus spp.) on incubating kingfishers may explain the lower survival of females than males, whereas juvenile birds may be especially vulnerable to predation by cats (Felis catus). Thus, conservation management for Tuamotu kingfishers should include use of metal guards on cavity trees to protect nests and incubating females, and control predator access during fledging periods. © 2012 The Wildlife Society.     

Density-dependent vital rates and their population dynamic consequences

We explore a set of simple, nonlinear, two-stage models that allow us to compare the effects of density dependence on population dynamics among different kinds of life cycles. We characterize the behavior of these models in terms of their equilibria, bifurcations, and nonlinear dynamics, for a wide range of parameters. Our analyses lead to several generalizations about the effects of life history and density dependence on population dynamics. Among these are: (1) iteroparous life histories are more likely to be stable than semelparous life histories; (2) an increase in juvenile survivorship tends to be stabilizing; (3) density-dependent adult survival cannot control population growth when reproductive output is high; (4) density-dependent reproduction is more likely to cause chaotic dynamics than density dependence in other vital rates; and (5) changes in development rate have only small effects on bifurcation patterns. Received: 12 April 1999 / Published online: 3 August 2000     

Are certain life histories particularly prone to local extinction?

Using stochastic simulations and elasticity analysis, we show that there are inherent differences in the risk of extinction between life histories with different demographies. Which life history is the most vulnerable depends on which vital rate varies. When juvenile survival varies semelparous organisms with delayed reproduction are the most vulnerable ones, while a varying developmental rate puts a greater threat to semelparous organisms with rapid development. Iteroparous organisms are the most vulnerable ones when adult survival varies. Generally, we do not expect to observe organisms in nature having variation in vital rates that produce a high risk of extinction. Given the results here we therefore predict that iteroparous organisms should show low variation in adult survival. Moreover, we predict that semelparous organisms should show low variation in juvenile survival and low variation in developmental rate. The effect of temporal correlation on extinction risk is most pronounced in organisms with semelparous life histories.     

Dramatic shifts in the gene pool of a managed population of an endangered species may be exacerbated by high genetic load

The Devils Hole pupfish, Cyprinodon diabolis, is restricted to a small habitat in southwestern Nevada. In 1972 the species was federally listed as an endangered species. Management efforts to mitigate extinction risks have been plagued by the inability to propagate the species in aquaria—anomalous for the genus—and repeated failure of propagation attempts in large, outdoor, artificial pools designed to mimic natural conditions in Devils Hole. These difficulties indicate that the species either has niche requirements that are not adequately recreated under artificial conditions or that it harbors a relatively large genetic load of deleterious mutations that compromises propagation. We used variation at 12 microsatellite loci to evaluate the results of natural, uncontrolled hybridization involving a population of C. diabolis inhabiting an artificial pool and invaders from a nearby population of the closely related C. nevadensis. The results suggest that following invasion of the pool by three C. nevadensis individuals, the gene pool underwent a rapid shift from pure C. diabolis to one comprised mostly of C. nevadensis alleles. Alleles diagnostic for C. nevadensis increased from about 0.03 to an average of 0.76 across four diagnostic loci over the course of 8 years or less. Although we cannot exclude explanations based on adaptation to Devils Hole, genetic drift, or demographic variability, these results and various other aspects of the biology of C. diabolis are best explained by the genetic load hypothesis. The work suggest avenues for future experimental work to evaluate these possibilities directly and provide an explanation for why some previous propagation efforts designed to mitigate extinction risk have failed.     

Winter weather affects asp viper Vipera aspis population dynamics through susceptible juveniles

Detailed studies on mammals and birds have shown that the effects of climate variation on population dynamics often depend on population composition, because weather affects different subsets of a population differently. It is presently unknown whether this is also true for ectothermic animals such as reptiles. Here we show such an interaction between weather and demography for an ectothermic vertebrate by examining patterns of survival and reproduction in six populations of a threatened European snake, the asp viper ( Vipera aspis ), over six to 17 years. Survival was lowest among juvenile and highest among adult snakes. The estimated annual probability for females to become gravid ranged from 26% to 60%, and was independent of whether females had reproduced in the year before or not. Variation in juvenile survival was strongly affected by winter temperature, whereas adult survival was unaffected by winter harshness. A matrix population model showed that winter weather affected population dynamics predominantly through variation in juvenile survival, although the sensitivity of the population growth rate to juvenile survival was lower than to adult survival. This study on ectothermic vipers revealed very similar patterns to those found in long-lived endothermic birds and mammals. Our results thus show that climate and life history can interact in similar ways across biologically very different vertebrate species, and suggest that these patterns may be very general.     

Sex- and age-dependent effects of population density on life history traits of red deer Cervus elaphus in a temperate forest

We studied both the short‐ and long‐term effects of density on three life history traits of a red deer population inhabiting a temperate forest. Both male and female body mass increased when population density decreased, but male mass changed to a greater extent than female mass. Density did not influence female survival irrespective of age, however, survival of males was lower at high density for all age classes except the prime‐age class. Pregnancy rates of primiparous females increased markedly with decreasing density, whereas those of adult hinds were fairly constant and unrelated to density. For both sexes, of the studied life history traits we detected a long‐term effect of density at birth (cohort effect) only on body mass. These results suggest that density influences life history traits in the same way as factors of environmental variation such as climate. In this population we did not find any evidence for an influence of climatic conditions on life history traits of red deer. Both mild winters and the absence of summer droughts during the study period could account for such an absence of climatic effects. We interpreted our results to show that 1) as expected for a highly dimorphic and polygynous species such as red deer, male traits showed consistently higher sensitivity to variation in density than female traits, illustrating possible costs caused by sexual selection in males, 2) the female‐based Eberhardt's model according to which increasing density should sequentially affect juvenile survival, reproductive rates of primiparous females, reproductive rates of adults and lastly adult survival was only partly supported because we found that pregnancy rate of primiparous females rather than juvenile survival was the most sensitive trait to variation in density. We propose that including variation in male traits would improve the accuracy of models of population dynamics of large mammals, at least for highly dimorphic species. Because the population we studied was not fenced, we only measured apparent survival. We discuss how dispersal, in relation to the phenotypic quality of young deer, might be a potential regulating factor under such conditions.     

Evaluating an icon of population persistence: the Devil's Hole pupfish

The Devil''s Hole pupfish Cyprinodon diabolis has iconic status among conservation biologists because it is one of the World''s most vulnerable species. Furthermore, C. diabolis is the most widely cited example of a persistent, small, isolated vertebrate population; a chronic exception to the rule that small populations do not persist long in isolation. It is widely asserted that this species has persisted in small numbers (less than 400 adults) for 10 000–20 000 years, but this assertion has never been evaluated. Here, we analyse the time series of count data for this species, and we estimate time to coalescence from microsatellite data to evaluate this hypothesis. We conclude that mean time to extinction is approximately 360–2900 years (median 410–1800), with less than a 2.1% probability of persisting 10 000 years. Median times to coalescence varied from 217 to 2530 years, but all five approximations had wide credible intervals. Our analyses suggest that Devil''s Hole pupfish colonized this pool well after the Pleistocene Lakes receded, probably within the last few hundred to few thousand years; this could have occurred through human intervention.     

Equal nonbreeding period survival in adults and juveniles of a long‐distant migrant bird

In migrant birds, survival estimates for the different life‐history stages between fledging and first breeding are scarce. First‐year survival is shown to be strongly reduced compared with annual survival of adult birds. However, it remains unclear whether the main bottleneck in juvenile long‐distant migrants occurs in the postfledging period within the breeding ranges or en route. Quantifying survival rates during different life‐history stages and during different periods of the migration cycle is crucial to understand forces driving the evolution of optimal life histories in migrant birds. Here, we estimate survival rates of adult and juvenile barn swallows (Hirundo rustica L.) in the breeding and nonbreeding areas using a population model integrating survival estimates in the breeding ranges based on a large radio‐telemetry data set and published estimates of demographic parameters from large‐scale population‐monitoring projects across Switzerland. Input parameters included the country‐wide population trend, annual productivity estimates of the double‐brooded species, and year‐to‐year survival corrected for breeding dispersal. Juvenile survival in the 3‐week postfledging period was low (S = 0.32; SE = 0.05), whereas in the rest of the annual cycle survival estimates of adults and juveniles were similarly high (S > 0.957). Thus, the postfledging period was the main survival bottleneck, revealing the striking result that nonbreeding period mortality (including migration) is not higher for juveniles than for adult birds. Therefore, focusing future research on sources of variation in postfledging mortality can provide new insights into determinants of population dynamics and life‐history evolution of migrant birds.     

Comparative survival and recovery of Ross's and lesser snow geese from Canada's central arctic

Large increases in several populations of North American arctic geese have resulted in ecosystem-level effects from associated herbivory. Consequently, some breeding populations have shown density dependence in recruitment through declines in food availability. Differences in population trajectories of lesser snow geese (Chen caerulescens caerulescens; hereafter snow geese) and Ross's geese (C. rossii) breeding in mixed-species colonies south of Queen Maud Gulf (QMG), in Canada's central arctic, suggest that density dependence may be limiting snow goose populations. Specifically, long-term declines in age ratios (immature:adult) of harvested snow geese may have resulted from declines in juvenile survival. Thus, we focused on juvenile (first-year) survival of snow and Ross's geese in relation to timing of reproduction (annual mean nest initiation date) and late summer weather. We banded Ross's and snow geese from 1991 to 2008 in the QMG Migratory Bird Sanctuary. We used age-structured mark-recapture models to estimate annual survival rates for adults and juveniles from recoveries of dead birds. Consistent with life history differences, juvenile snow geese survived at rates higher than juvenile Ross's geese. Juvenile survival of both species also was lower in late seasons, but was unrelated to arctic weather measured during a 17-day period after banding. We found no evidence of density dependence (i.e., a decline in juvenile survival over time) in either species. We also found no interspecific differences in age-specific hunting vulnerability, though juveniles were more vulnerable than adults in both species, as expected. Thus, interspecific differences in survival were unrelated to harvest. Lower survival of juvenile Ross's geese may result from natural migration mortality related to smaller body size (e.g., greater susceptibility to inclement weather or predation) compared to juvenile snow geese. Despite lower first-year survival, recruitment by Ross's geese may still be greater than that by snow geese because of earlier sexual maturity, greater breeding propensity, and higher nest success by Ross's geese. © 2012 The Wildlife Society.     

Periodic dynamics in a two-stage Allee effect model are driven by tension between stage equilibria

Single species difference population models can show complex dynamics such as periodicity and chaos under certain circumstances, but usually only when rates of intrinsic population growth or other life history parameter are unrealistically high. Single species models with Allee effects (positive density dependence at low density) have also been shown to exhibit complex dynamics when combined with over-compensatory density dependence or a narrow fertility window. Here we present a simple two-stage model with Allee effects which shows large amplitude periodic fluctuations for some initial conditions, without these requirements. Periodicity arises out of a tension between the critical equilibrium of each stage, i.e. when the initial population vector is such that the adult stage is above the critical value, while the juvenile stage is below the critical value. Within this area of parameter space, the range of initial conditions giving rise to periodic dynamics is driven mainly by adult mortality rates. Periodic dynamics become more important as adult mortality increases up to a certain point, after which periodic dynamics are replaced by extinction. This model has more realistic life history parameter values than most 'chaotic' models. Conditions for periodic dynamics might arise in some marine species which are exploited (high adult mortality) leading to recruitment limitation (low juvenile density) and might be an additional source of extinction risk.     

Elasticity Analysis of Green Sturgeon Life History

I provide an analysis of a simplified life history model for green sturgeon, Acipenser medirostris, based on published and recent estimates of reproduction and growth rates and survival rates from life history theory. The deterministic life cycle models serve as a tool for qualitative analysis of the impacts of perturbations on green sturgeon, including harvest regulations based on minimum and maximum size limits (“slot limits”). Elasticity analysis of models with two alternative age–length relationships give similar results, with a high sensitivity of population growth rate to changes in the survival rate of subadult and adult fish. A dramatic increase in the survival of young of the year sturgeon or annual egg production is required to compensate for relatively low levels of fishing mortality. Peak reproductive values occur from ages 25 to 40. An increase or decrease in the maximum and minimum size limits can have a profound effect on the elasticity of population growth to changes in the annual survival rate of age classes specified by the slot, due to changes in the number of age classes of subadults and adults that are available for harvest. This analysis provides managers with a simple tool to assess the relative impacts of alternative harvest regulations. In general, green sturgeon follow life history patterns similar to other sturgeon, but species-specific demographic information is needed to produce more complex assessment and viability analysis models.     

Indeterminate growth in long-lived freshwater turtles as a component of individual fitness

Although evidence that reptiles exhibit indeterminate growth remains equivocal and based on inadequate data, the assumption that they do is still widely accepted as a general trait of reptiles. We examined patterns of variation in adult growth using long-term mark-recapture data on 13 populations of 9 species representing 3 families of freshwater turtles located in South Carolina, Michigan, and Arizona in the USA and in Ontario, Canada. Across 13 study populations, growth rates of all adults and only those that grew averaged 1.5 and 1.9 mm/yr respectively. Sources of variation in growth rates included species, population, sex, age, and latitude. Most adults of both sexes with recapture intervals greater than 10 years grew, but across all populations an average of 19 % of individuals did not grow (some with recapture intervals up to 30 years). For known-age adults of three species, the highest growth rates occurred during the 10 years following sexual maturity, and the proportions of non-growing individuals increased with age. Growth rates of adults were on average 92 % lower than those of juveniles. Based on linear relationships of clutch size and body size of females at average juvenile and adult growth rates it would take 0.7 (0.2–1.2) years and 8.6 (min–max = 2.3–18.5) years, respectively, to grow enough to increase clutch size by one egg. The majority of within population variation in adult body size in 3 species appeared to be a combination of differences in ages at maturity and juvenile and early adult growth, rather than indeterminate growth. The results from our study populations indicate that increases in body size (and associated reproductive output) that results from indeterminate growth are not substantial enough to represent a major factor in the evolution of life histories in general or the evolution of longevity and aging specifically.     

Environmental networks,compensating life histories and habitat selection by white-footed mice

Summary Analysis of 6 years' data on a population of free-living white-footed mice documents both phenotypic and environmental control of litter size. Litter size was positively correlated with maternal body size. Maternal size depended upon both seasonal and annual variation. Paradoxically, the proportion of small versus large litters varied among habitats independently of the effects of body size. The result is an influence of habitat on life history that yields patterns of reproduction and survival opposite to the predictions of demographic theory. The habitat producing the largest litters had a relatively high ratio of adult/juvenile survival. Litter size was small in the habitat where the adult/juvenile survival ratio was smallest. All of these anomalous patterns can be explained through density-dependent habitat selection by female white-footed mice. Life-history studies that ignore habitat and habitat selection may find spurious correlations among traits that result in serious misinterpretations about life history and its evolution.