Dynamics of a declining amphibian metapopulation: Survival, dispersal and the impact of climate

Climate can interact with population dynamics in complex ways. In this study we describe how climatic factors influenced the dynamics of an amphibian metapopulation over 12 years through interactions with survival, recruitment and dispersal. Low annual survival of great crested newts (Triturus cristatus) was related to mild winters and heavy rainfall, which impacted the metapopulation at the regional level. Consequently, survival varied between years but not between subpopulations. Despite this regional effect, the four subpopulations were largely asynchronous in their dynamics. Three out of the four subpopulations suffered reproductive failure in most years, and recruitment to the metapopulation relied on one source. Variation in recruitment and juvenile dispersal was therefore probably driving asynchrony in population dynamics. At least one subpopulation went extinct over the 12 year period. These trends are consistent with simulations of the system, which predicted that two subpopulations had an extinction risk of >50% if adult survival fell below 30% in combination with low juvenile survival. Intermittent recruitment may therefore only result in population persistence if compensated for by relatively high adult survival. Mild winters may consequently reduce the viability of amphibian metapopulations. In the face of climate change, conservation actions may be needed at the local scale to compensate for reduced adult survival. These would need to include management to enhance recruitment, connectivity and dispersal.     

The ecology of extinction: population fluctuation and decline in amphibians

Even among widespread species with high reproductive potentials and significant dispersal abilities, the probability of extinctions should be correlated both with population size variance and with the extent of population isolation. To address how variation in demographic characteristics and habitat requirements may reflect on the comparative risk of species decline, I examined 617 time series of population census data derived from 89 amphibian species using the normalized estimate of the realized rate of increase, ΔN, and its variance. Amphibians are demonstrably in general decline and exhibit a great range of dispersal abilities, demographic characteristics, and population sizes. I compared species according to life-history characteristics and habitat use. Among the populations examined, census declines outnumbered increases yet the average magnitudes for both declines and increases were not demonstrably different, substantiating findings of amphibian decline. This gives no support for the idea that amphibian population sizes are dictated by regimes featuring relatively rare years of high recruitment offset by intervening years of gradual decline such that declines may outnumber increases without negative effect. For any given population size, those populations living in large streams or in ponds had significantly higher variance than did populations of completely terrestrial or other stream-dwelling amphibians. This could not be related to life-history complexity as all the stream-breeding species examined have larvae and all of the wholly terrestrial species have direct development without a larval stage. Variance in ΔN was highest amongst the smallest populations in each comparison group. Estimated local extinction rates averaged 3.1% among pond-breeding frogs, 2.2% for pond-breeding salamanders, and negligible for both stream-breeding and terrestrial direct-developing species. Recoveries slightly exceeded extinctions among European pond-breeding frogs but not among North American pond-breeding frogs. Less common species had greater negative disparities between extinctions and recoveries. Species with highly fluctuating populations and high frequencies of local extinctions living in changeable environments, such pond- and torrent-breeding amphibians, may be especially susceptible to curtailment of dispersal and restriction of habitat.     

Potential factors controlling the population viability of newly introduced endangered marble trout populations

While several population viability analyses (PVAs) have been performed on anadromous salmonids, less attention has been given to stream-living salmonids. In this work, we explore the role of PVA as a tool in the recovery of threatened stream-living salmonid species. The analysis has been performed with reference to marble trout Salmo marmoratus, a salmonid with a limited geographic distribution and at risk of extinction due to hybridization with the non-native introduced brown trout. Demographic parameters, such as survival, fecundity and density-dependent patterns were estimated from an eight year on-going monitoring program of two translocated marble trout populations in pristine, previously fishless streams (Zakojska and Gorska) in the Soca and Idrijca river basins (Slovenia). To explore the importance of disturbance events such as floods on marble trout population dynamics, we performed a PVA under three scenarios: (1) occurrence of both severe and moderate floods; (2) occurrence of only moderate floods; (3) no flood events. Our analysis shows that population viability is threatened only by severe flood events, otherwise the two populations prove to be fairly stable with population abundance fluctuating around stream carrying capacity. A sensitivity analysis performed on model parameters highlighted that density-dependence in first-year survival and the magnitude of reduction in population size after a severe flood are the two most crucial parameters affecting population abundance and quasi-extinction probability, respectively. While only extreme floods can drive the population to extinction, the increase in juvenile survival when population abundance collapses after a major flood may allow the populations to quickly recover from few reproductive individuals back to stream carrying capacity.     

The genetic structure of coastal giant salamanders (Dicamptodon tenebrosus) in a managed forest

The salamander, Dicamptodon tenebrosus, is threatened by habitat loss and fragmentation associated with forest harvest activities. We used three microsatellite loci and 38 amplified fragment length polymorphisms (AFLPs) to quantify population structure and indirectly evaluate the impacts of forest harvesting on this species. We sampled two old growth sites, three second growth sites and three recently clearcut sites in British Columbia, Canada. Microsatellite allelic richness and the percentage of polymorphic AFLPs were positively correlated with the age of forest stands. Similarly, heterozygosity estimated from both marker types was positively correlated with stand age. Population subdivision (F_st) estimated among forested sites using microsatellite and AFLP markers was 0.033 and 0.095, respectively. Lower genetic variation and heterozygosity in recent clearcuts suggest that clearcut logging may be associated with local population declines. Our genetic findings are consistent with previous studies that report lower salamander densities in recently clearcut sites.     

Long-term monitoring of tropical bats for anthropogenic impact assessment: Gauging the statistical power to detect population change

Bats are ecologically important mammals in tropical ecosystems; however, their populations face numerous environmental threats related to climate change, habitat loss, fragmentation, hunting, and emerging diseases. Thus, there is a pressing need to develop and implement large-scale networks to monitor trends in bat populations over extended time periods. Using data from a range of Neotropical and Paleotropical bat assemblages, we assessed the ability for long-term monitoring programs to reliably detect temporal trends in species abundance. We explored the magnitude of within-site temporal variation in abundance and evaluated the statistical power of a suite of different sampling designs for several different bat species and ensembles. Despite pronounced temporal variation in abundance of most tropical bat species, power simulations suggest that long-term monitoring programs (?20 years) can detect population trends of 5% per year or more with adequate statistical power (?0.9). However, shorter monitoring programs (?10 years) have insufficient power for trend detection. Overall, our analyses demonstrate that a monitoring program extending over 20 years with four surveys conducted biennially on five plots per monitoring site would have the potential for detecting a 5% annual change in abundance for a suite of bat species from different ensembles. The likelihood of reaching adequate statistical power was sensitive to initial species abundance and the magnitude of count variation, stressing that only the most abundant species in an assemblage and those with generally low variation in abundance should be considered for detailed population monitoring.     

Flawed population viability analysis can result in misleading population assessment: A case study for wolves in Algonquin park, Canada

For many populations and species, population viability analysis (PVA) plays a critical role in developing defensible conservation strategies and recovery plans. Although technical aspects of PVA have been well scrutinized, misapplication of PVA and misinterpretation of its results have received less attention. To illustrate potential hazards of improper use of PVA we reanalyzed data from a recent study on viability of wolves in Algonquin Provincial Park (APP), Ontario, Canada. The original PVA predicted extirpation of wolves from APP and prompted both a ban on wolf harvesting in a 10-16 km buffer zone surrounding the 7571 km² park and an intensive research program to evaluate efficacy of the ban. Our reanalysis showed that limited and imprecise wolf population density and demographic rate estimates, as well as flawed population assessment and reconstruction methods, led to overly pessimistic evaluation of wolf population status in APP. In fact, our analyses suggest that wolves in APP are unlikely to decline significantly over the next 20 years. Further, contrary to earlier conclusions we suggest that rapid wolf population recovery following protection from human exploitation would be likely and readily detectable. These findings highlight the need for adequate data, appropriate methodology, and proper analytical context when conducting PVA. Because the original PVA prompted substantial redirection of staff and financial resources from other significant conservation initiatives, we conclude that improper PVA may undermine execution of effective wildlife management and ultimately provide a disservice to conservation biology.     

Spatial analysis of habitat quality in a fragmented population of little bustard (Tetrax tetrax): Implications for conservation

Little bustard populations have suffered reduction and isolation as a consequence of landscape transformations resulting from changes in traditional agricultural systems. Consequently, the species survives within reduced and fragmentary habitats, like islands isolated in a modified matrix. In this paper, we analyze the spatial variations in male density and habitat quality in a fragmented population located at the limit of the species’ Iberian range, which is affected by agricultural intensification, using a regional modelling approach. Habitat quality (quantified according to the species perception) and bird density decreased along the intensification gradient. However, in the most intensive agricultural zone, the quality of habitats selected by little bustard males increased, while density decreased, against the expected. In possible explanation, we suggest: (1) density is not necessarily a good indicator of habitat quality, (2) population could be under-saturated in this zone, (3) interannual variations in species distribution, or (4) other relevant variables related to the agricultural intensification process not included in this analysis, such as small-scale disturbances. Analysis of population distribution pattern showed a spatial configuration in which the most densely populated squares were located at the core of the biggest population patches, in contact with mid-density squares, and all surrounded by low-density squares. Fragmentation negatively affected habitat quality and male density. Largest population patches, containing higher density values, were located at the beginning of the intensification gradient. Preservation of little bustard densities is related to an adequate management of the farming system. Habitat fragmentation requires an urgent conservation strategy to prevent local and regional scale habitat deterioration, by reducing patch isolation to maintain genetic diversification and functional connectivity.     

Optimising biodiversity assessments by volunteers: The application of occupancy modelling to large-scale amphibian surveys

Mobilising volunteers to carry out biodiversity assessments can help to identify priorities for conservation across broad geographical scales. However, even when volunteers carry out simple presence-absence surveys, there can be significant issues over false absences and subsequent data interpretation. Simple but scientifically robust protocols are therefore required for these programmes. Here we evaluate amphibian survey protocols for the National Amphibian and Reptile Recording Scheme (NARRS) in Britain, which aims to assess the status of five widespread amphibian species. Surveys were undertaken by trained volunteers and researchers in two contrasting landscapes over 2 years, and occupancy modelling was used to determine covariates of detection, and to optimise the number of surveys and number of methods required. Although surveys need to take into account seasonal and annual changes in the detectability of different species, there were also landscape effects. Frogs and toads were generally harder to detect in ponds in Kent than in Wales, while the converse was true of newts. Adding bottle-trapping to the suite of methods increased the detection of smooth and palmate newts in both areas, and of great crested newts in Wales. Overall, reliable assessment of the presence or absence of all five species at a site required four separate surveys, each using four different methods (visual encounter surveys during both day and night, dip netting and bottle-trapping). Our approach may prove useful for finding the best compromises between rigor and simplicity when volunteers are used in large-scale surveys.     

The influence of uncertainty on conservation assessments: Australian frogs as a case study

We evaluated the influence of uncertainty, based on variation in expert opinion, on assessment of conservation status of Australian amphibians. We examined relationships between different biological variables and inferred relative extinction risk, the influence of uncertainty on resulting ranks, and regional patterns of extinction risk and uncertainty. Our results were in general agreement with the International Union for the Conservation of Nature and Natural Resources but also reveal apparent high extinction risks among some taxa that the IUCN did not classify in any threatened category. These differences were exaggerated when the most conservative status assessments were taken from variation in expert opinion. Our assessments of relative extinction risk were strongly dependent on basic demographic variables, particularly population size, geographic distribution of populations and age at first reproduction. We identified regional hotspots of high relative extinction risk and poor knowledge of amphibians, leading to high uncertainty about the conservation status of species from those areas. Regional clustering of species with high relative extinction risk and high uncertainty may indicate higher levels of relative extinction risk than previously assessed. Our results highlight the influence of uncertainty on interpretation of conservation assessments of organism groups with large knowledge gaps. Uncertainty should be further incorporated into conservation planning as it not only highlights taxa with potentially underestimated extinction risk, but also facilitates identification of knowledge gaps informative of conservation status. Knowledge of regional patterns of extinction risk and uncertainty assists conservation planning through identification of regions of high extinction risk and/or large knowledge gaps.     

Stochastic variation in reproductive success of a rare frog, Rana sevosa: implications for conservation and for monitoring amphibian populations

Although amphibian populations are thought to be declining in many parts of the world, detailed information on populations in decline are often not available. From 1988 to 2001, we studied temporal variation in the reproductive biology of the only known population of dusky gopher frogs, Rana sevosa Goin and Netting. We found high annual variation in reproductive effort, mortality at the egg and larval stages, and hydroperiod length. No overall trends were apparent in terms of either number of egg masses deposited or in reproductive success, as we found extensive variation among years in the number of egg masses deposited, a high rate of reproductive failure, and no consistent relationship between the number of females present, the number of eggs deposited, and the number of metamorphs emerging. Given the complete isolation of this population from other gopher frogs and the high rate of reproductive failure, the probability of extinction of this population appears to be quite high (0.125-0.316).     

The use of historical collections to estimate population trends: A case study using Swedish longhorn beetles (Coleoptera: Cerambycidae)

Long term data to estimate population trends among species are generally lacking. However, Natural History Collections (NHCs) can provide such information, but may suffer from biases due to varying sampling effort. To analyze population trends and range-abundance dynamics of Swedish longhorn beetles (Coleoptera: Cerambycidae), we used collections of 108 species stretching over 100 years. We controlled for varying sampling effort by using the total number of database records as a reference for non-red-listed species. Because the general frequency of red-listed species increased over time, a separate estimate of sampling effort was used for that group. We observed large interspecific variation in population changes, from declines of 60% to several hundred percent increases. Most species showed stable or increasing ranges, whereas few seemed to decline in range. Among increasing species, rare species seemed to expand their range more than common species did, but this pattern was not observed in declining species. Historically, rare species did not seem to be at larger risk of local extinction, and population declines were mostly due to lower population density and not loss of sub-populations. We also evaluated the species’ declines under IUCN red-list criterion A, and four currently not red-listed species meet the suggested threshold for Near Threatened (NT). The results also suggested that species’ declines may be overlooked if estimated only from changes in species range.     

Large scale risk-assessment of wind-farms on population viability of a globally endangered long-lived raptor

Wind-farms receive public and governmental support as an alternative energy source mitigating air pollution. However, they can have adverse effects on wildlife, particularly through collision with turbines. Research on wind-farm effects has focused on estimating mortality rates, behavioural changes or interspecific differences in vulnerability. Studies dealing with their effects on endangered or rare species populations are notably scarce. We tested the hypothesis that wind-farms increase extinction probability of long-lived species through increments in mortality rates. For this purpose, we evaluate potential consequences of wind-farms on the population dynamics of a globally endangered long-lived raptor in an area where the species maintains its greatest stronghold and wind-farms are rapidly increasing. Nearly one-third of all breeding territories of our model species are in wind-farm risk zones. Our intensive survey shows that wind-farms decrease survival rates of this species differently depending on individual breeding status. Consistent with population monitoring, population projections showed that all subpopulations and the meta-population are decreasing. However, population sizes and, therefore, time to extinction significantly decreased when wind-farm mortality was included in models. Our results represent a qualitative warning exercise showing how very low reductions in survival of territorial and non-territorial birds associated with wind-farms can strongly impact population viability of long-lived species. This highlights the need for examining long-term impacts of wind-farms rather than focusing on short-term mortality, as is often promoted by power companies and some wildlife agencies. Unlike other non-natural causes of mortality difficult to eradicate or control, wind-farm fatalities can be lowered by powering down or removing risky turbines and/or farms, and by placing them outside areas critical for endangered birds.     

Matrix analysis to evaluate sustainability: The tropical tree Aquilaria crassna, a heavily poached source of agarwood

We used size-structured Lefkovitch projection matrix analysis to predict future trends in the survival of Aquilaria crassna (Thymelaeaceae), a tropical evergreen forest tree that has been highly sought after for its valuable aromatic wood (agarwood) for millennia. Data on growth, damage to trees by poachers, fruit production, seed dispersal and seedling recruitment were collected from a 30-ha plot in Khao Yai National Park, central Thailand that had seen moderate poaching. The population asymptotic growth rate, λ_a, and transient growth rate, λ_tr, found from using the matrix to project the observed population 48 years, were 1.002 and 1.005, respectively, with 95% confidence intervals of [0.985, 1.016] and [0.985, 1.023]. The stable size distribution obtained from the matrix was reasonably similar to the observed size distribution, suggesting that at the time of the study the population was not far from equilibrium. Sensitivity analysis and simulations of poaching on adult trees indicate that both λ’s are very sensitive to the removal of adult trees and the growth of preadult trees. In particular, the increase in tree mortality and decrease in preadult growth rate caused by agarwood collection seen in some areas could cause extirpation of the population. While in such cases the population appears to be poised on the brink of decline, several factors that we could not evaluate could alter its fate. First, adult deaths could stimulate recruitment of young under the parent trees; second, there is marked year-to-year variation in fruiting success and possibly recruitment; third, there is considerable spatial variation in tree density and recruitment, suggesting that attempts to evaluate future success need to encompass larger spatial and time scales.     

Integrating effects of hunting policy, catastrophic events, and inbreeding depression, in PVA simulation: the Scandinavian wolf population as an example

Focusing on the wolf Canis lupus in Scandinavia as an example, criteria are proposed and an analysis performed to assess the effect on extinction risk of various control policies, while accounting simultaneously for effects of inbreeding depression and potential catastrophic events. Each control policy is characterized by a hunting pressure (the increase caused by hunting of annual mortality rates) combined with a hunting threshold (the population size below which hunting is not permitted). Catastrophes are taken into account by including the persistence of a severe catastrophe in the criterion for population viability. Based on these criteria, the results suggest that only a very limited amount of hunting should be permitted at low population sizes. The results also illustrate the importance of including a long-term perspective in modelling threatened populations.     

Management recommendations based on matrix projection models: The importance of considering biological limits

Matrix population models are a common tool for evaluating different management strategies. In general, under deterministic analyses, management strategies are recommended that improve those matrix transitions that are most sensitive or elastic with respect to the asymptotic population growth rate, λ. These recommendations usually ignore the biological limit for these transitions. In this paper we use the endangered Serengeti cheetah (Acinonyx jubatus) as a case study to illustrate that ignoring biological limits leads to a recommendation that will not always achieve the desired goal of an asymptotic population growth rate, λ ? 1.We estimate the survivorships of adult cheetahs in captivity using cheetah studbook data, which is a conservative estimate of the biological limit for the adult survivorship of wild cheetahs. Our analysis suggests that adult survival sharply decreases after 8.5 years. In addition, captive cheetahs older than 18 years do not reproduce. We modify a previously published population projection matrix to include the effect of senescence on survival and fecundity. Our model suggests that increasing adult survivorship alone is not sufficient to reverse population decline. However, an additional small increase in newborn survival is likely to result in a viable cheetah population. We show these conclusions hold even in the presence of relatively large parameter perturbations.     

Long-term trends in the abundance of Mediterranean wetland vertebrates: From global recovery to localized declines

Biodiversity loss is unevenly distributed in space and time. Species have reached critically low population sizes in some areas, and remain abundant in others. Similarly, some species may benefit from successful conservation plans, while others still experience severe population depletions driven by negative impacts of human activities. Although several indicators have been proposed to measure the fate of biodiversity, they are generally only implemented globally so their relevance for regional assessment is still unclear. Here, we calculated the first regional trend in the Living Planet Index for the Mediterranean wetlands (Med LPI), an indicator that summarizes the fate of global biological diversity based on the temporal trends in abundance of vertebrate populations. The Med LPI was based on 1641 vertebrate populations of 311 species recorded in Mediterranean wetlands from 1970–2008, in 27 different countries. We investigated whether trends in the Med LPI differed between eastern and western Mediterranean countries, which have different socio-economic contexts. Finally, we assessed whether and how the trend in the Med LPI was robust to changes in the number and identity of species considered. We found that, at the Mediterranean scale, the Med LPI increased steeply, which could be taken at first sight, as a general recovery of wetland biodiversity in this biogeographical region. However, we found highly contrasting spatial trends within the Mediterranean region: the average trend was positive for western and negative for eastern countries. Moreover, we showed that depending on the method used to estimate the trend in Med LPI, it can be sensitive to the number and identity of the species considered. We suggest that understanding the regional discrepancies of the trend in biodiversity indicators as well as their robustness to the species represented in the index will enhance progress assessment towards global and regional conservation strategies.     

Incorporating spatial structure and stochasticity in endangered Bonelli’s eagle’s population models: Implications for conservation and management

Population models have played a chief role informing management decisions for the endangered Bonelli’s eagle (Aquila fasciata) in Spain. In this paper, we incorporate spatial structure and stochasticity in the construction of individual-based metapopulation models, and use these models to explore the effects of possible management actions on the persistence of the species in Spain. To build the models we used data on seven sub-populations that have experienced different trends in the last decades, and we introduced new estimates of pre-adult survival rate. The elasticity analysis of our models showed that when the interchange of individuals among sub-populations is taken into account, pre-adult mortality plays the key role in determining the overall population trend. This is in contrast to what it has been suggested by previous demographic models that modelled local populations as isolated. Specifically, a 20% decrease in pre-adult mortality during the first two years of life was enough for the stabilization of the metapopulation (i.e., λ  1.0). However, neither a similar decrease in the values of adult mortality, nor an increase in the percentage of breeders, modified the declining trend of our model metapopulation. This reinforces the idea that to ensure the long-term persistence of the species in Spain, management actions should aim at minimizing pre-adult mortality. These include locating and protecting the areas used by juvenile Bonelli’s eagles (e.g., temporary settlements), minimizing the risk of electrocution in power lines, and preventing human persecution.     

Modelling the effect of El Niño on the persistence of small populations: The Galápagos penguin as a case study

Small populations are vulnerable to long-term declines, even where short-term censuses indicate increasing trends in numbers. Census data for the Galápagos penguin (Spheniscus mendiculus) collected between 1970 and 2004 provide evidence that despite year-to-year population increases detected in most of the annual censuses, the strong El Niño events of 1982-83 and 1997-98 were followed by population declines of more than 60% from which the species has yet to recover. Such large declines raise concerns about the future viability of the species because the frequency and severity of El Niño events are predicted to increase. We used the simulation software VORTEX to evaluate the potential effects of El Niño on the risk of extinction of the Galápagos penguin population and its four constituent subpopulations. Weak and strong El Niño events were treated as catastrophes, with varying frequencies, which simulated past, current and future effects on the penguin population. The “Current El Niño” scenario, based on the frequency of El Niño events recorded in the Galápagos between 1965 and 2004, indicated an approximately 30% probability of extinction within the next 100 years for the penguin population. More ominously, the species may be at a greater risk if the frequency of strong El Niño episodes increases only marginally. A probability of extinction greater than 80% was predicted when the current frequency (5%) of strong El Niño events was doubled (to 10%). The probabilities of extinctions were higher for each subpopulation treated individually, ranging from 34% for Isabela and Fernandina, 64% for Bartolomé-Santiago to 78% for the smallest subpopulation on Floreana. Sensitivity analyses identified survival of penguins during El Niño events and sex ratio as influential parameters. The estimates of extinction risk may be conservative as other threats associated with increased human activities on the islands may further compromise species persistence.     

The importance of understanding spatial population structure when evaluating the effects of silviculture on spotted salamanders (Ambystoma maculatum)

Current silvicultural practices in the northeastern United States create diverse vegetation patterns and microclimates that provide a mosaic of terrestrial habitats for amphibian species. We inferred patterns of habitat use by the spotted salamander, Ambystoma maculatum, by studying colonization of four newly created breeding pools each surrounded by four different forest treatments: a control, partial cut, clearcut with coarse woody debris (CWD) removed, and clearcut with CWD retained. Created pools were rapidly colonized, indicating that breeding salamanders readily bred in new pools they encountered. This suggests that in our study area pool-specific philopatry and site fidelity may not be high and that particular pools may not define local breeding populations. In the experimental silvicultural treatments, juvenile salamanders preferred the control forest to the clearcuts, whereas adult salamanders showed no significant preferences among the treatments. Although silvicultural practices such as clearcutting may reduce juvenile movement between pools, inter-pool movement by adults that are more tolerant of habitat change may ameliorate this effect in our study area. If juveniles are the primary life-history stage dispersing between local populations (i.e., moving between more isolated groups of pools), however, there is potential for clearcutting to reduce the connectivity between local populations.