Effect of land use and climate change on the future fate of populations of an endemic species in central Europe

The identification of optimal management strategies for a given species is a major challenge of species conservation. It becomes especially challenging when the environmental conditions are expected to change in the future, and the optimal management applied today may differ from the management that is optimal under the changed conditions (e.g. due to climate change).This study evaluates prospect of a rare plant species endemic to semi-natural grasslands in central Europe, Gentianella praecox subsp. bohemica. The number of populations of this species has declined rapidly in the last 60 years; currently, a conservation action plan has been established in the Czech Republic, where most populations of this species occur. This study uses periodic matrix models to compare different management regimes under different scenarios of climate change and to identify the optimal management in each case.Without management, populations of the species are not able to survive. Flowering individuals can occur for a long time after the cessation of management, but the extinction of the population is inevitable within several decades. Without management, even very large populations (1000 flowering individuals) will go extinct in less than 50 years. Total extinction (including seed bank) will follow several years after observation of the last flowering plant. The most suitable management is mowing and disturbance (by harrowing), which is also the best method for restoration of threatened populations. Mowing is less suitable, but it is fully sufficient for large prospering populations. When managed, even small populations (10–15 flowering individuals) are able to survive. When management is applied, future climate change may have a relatively small impact on the probability of survival of the species. Climate change will, however, increase the extinction probability of very small populations.     

Successful reintroductions of the endangered long-lived Sargent’s cherry palm, Pseudophoenix sargentii, in the Florida Keys

The 1991-1994 reintroductions of Florida endangered Pseudophoenix sargentii to 13 Florida Keys sites represent a rare example of a successful multi-agency long-term effort to conserve a long-lived palm. To assess reintroduction success, we compared population demographics with and without reintroduced plants and conducted population viability analyses. Since 1991, the wild population has increased 6.4-fold. Survival from 2000-2004 was 94%, growth was positive (λ = 1.013), and there was no predicted extinction risk. Recent wild population growth is attributed to good seedling recruitment and removing the greatest threats. After 14 years, reintroductions had 43% survival, increased total plants in the wild by 27%, and expanded the species’ distribution. Reintroduced plants had faster maturation rates, improved population age structure, and enhanced population growth (λ = 1.032). Success varied with transplant year, location, microsite, and original transplant size. Failures in 1991 and at some historic sites emphasize the need for a multi-year, multi-site approach to reintroductions to buffer against stochastic losses. Rockland hammocks and the tops of coastal berms had greatest plant growth and survival. Large transplants had the greatest survival. Because no reintroduced plants are reproductive, transitions between stages are extremely slow, and plants may require >30 years to mature, continued institutional dedication to long-term monitoring will be required to assess whether the populations are self-sustaining. Horticultural expertise and ex situ collections complimented support of land managing agencies for the species’ preservation. These first rare plant reintroductions to Florida State Parks opened avenues for more plant conservation efforts and public interpretation.     

Population viability of the narrow endemic Helianthemum juliae (CISTACEAE) in relation to climate variability

Narrow endemic plants are highly vulnerable to extinction as a result of human disturbance and climate change. We investigated the factors affecting the population viability of Helianthemum juliae, a perennial plant endemic to the Teide National Park on Tenerife, Canary Islands. One population was demographically monitored from 1992 to 2001 and analysed using matrix projection models to determine finite rates of increase and critical stages in the life cycle. Lambda values varied between 0.697 and 1.740, and were highly positively correlated with annual precipitation, but not with temperature. Survival of adults had the highest elasticity, and summed elasticities of the growth and fecundity transitions correlated positively with lambda and precipitation. Most of the mortality in the population seemed drought-related, and no other threats were identified. Deterministic simulations showed population increase, but introducing environmental stochasticity by modelling variation in precipitation from existing data of the past 85 years revealed high extinction probabilities (0.74-0.83 in the next 100 years). This plant is likely to be at risk under scenarios of global warming. Our simulations suggest that augmenting the population would only delay extinction. A more viable option for long-term conservation seems to be the introduction of populations at more humid locations within the Teide caldera.     

Effects of management regimes and extreme climatic events on plant population viability in Eryngium alpinum

Extreme climatic events like the 2003 summer heatwave and inappropriate land management can threaten the existence of rare plants. We studied the response of Eryngium alpinum, a vulnerable species, to this extreme climatic event and different agricultural practices. A demographic study was conducted in seven field sites between 2001 and 2010. Stage-specific vital rates were used to parameterize matrix population models and perform stochastic projections to calculate population growth rates and estimate extinction probabilities. Among management regimes, spring grazing and land abandonment decreased vital rates and population growth, while autumn grazing and late mowing had positive effects on population viability. The 2003 heatwave reduced fecundity rates and survival rates. Only spring grazed sites presented considerable extinction risk. Stochastic projections showed that an increased frequency of 2003-like events may exacerbate extinction risk, but extinction probability depends mainly on land management regimes. To better conserve E. alpinum populations, we recommend conversion of presently spring grazed and abandoned sites to late mowing or autumn grazing.     

Responses of cycads with different life histories to the impact of plant collecting: simulation models to determine important life history stages and population recovery times

Collection of plants and seeds from wild populations threatens a large number of cycad species. We investigated to what extent individual life history stages contribute to population growth (λ) and compared two species with major differences in life histories in the African genus Encephalartos: Encephalartos cycadifolius, a highly persistent grassland species that resprouts after fire, and Encephalartos villosus, a relatively fast growing, non-sprouting forest species. Several harvesting scenarios impacting different sized individuals were simulated to determine the sensitivity of the two functional types to harvesting. In both species λ was most sensitive to changes in abundance of adult plants. The harvesting of seeds had minimal impact on population growth rates, whereas harvesting of adult plants led to rapid population decline. This response from two very different functional types suggests that the conservation of adult plants is critical for all cycad species. Despite similar responses to adult mortality, the two species had substantially different population growth rates. This determined recovery time after harvesting of adult individuals. Encephalartos cycadifolius is typical of highly persistent plant species associated with low levels of recruitment and unable to recover from even small losses of adults within a reasonable conservation time frame (<100 years). Our results suggest that the ability to recover from loss of individuals is an important factor that should be considered when assessing the vulnerability of wild populations to threats.     

Two-sex population projection of the endemic and dioecious rainforest shrub, Gardenia actinocarpa (Rubiaceae)

Gardenia actinocarpa (Rubiaceae)—an endemic and dioecious shrub-small tree of the lowland rainforest of Cape Tribulation, NE Australia—is evaluated for its long-term population persistence using five-year demographic data from three permanent plots of the species. Two-sex, size-specific Lefkovitch matrices were constructed to evaluate the species’ vital rates and extinction thresholds. One site indicated a sign of significant population growth (annual λ=1.056), while the remaining two gave λs close to unity (λ=1.0102 and 1.007). Overall, λ was greater than 1 (λ=1.0281) indicating that G. actinocarpa will increase in population size with time, though male plants were projected to grow faster in number than female plants. Elasticity analyses indicated that the largest size class (>22 cm diameter) made the greatest contribution to population growth (28%), especially the male plants (23%). Also λ was equally sensitive to survival/stasis (45%) and growth (44%) and least sensitive to fecundity (11%). Stochastic simulations gave 0.505 probability of quasi-extinction to 10% of its initial size in 100 years of population growth projection- suggesting that the endemic G. actinocarpa, despite a positive rate of population increase, is indeed threatened. Sensitivity analyses and numerical simulations showed that to maintain population persistence of G. actinocarpa, efforts should concentrate, following cost-benefit analyses, on increasing seed production coupled with enhancing establishment of individuals in the seedling, juvenile and vegetative phases.     

Integrating demographic and genetic approaches in plant conservation

We summarize the problems that populations of formerly common plants may encounter when habitat fragmentation isolates them and reduces population size. Genetic erosion, inbreeding depression, Allee-effects on reproductive success, catastrophes and environmental stochasticity are illustrated with studies on species that have recently become rare in The Netherlands due to habitat fragmentation. These clearly indicate that population viability is negatively affected. We also show that in the recent literature (since 1980), most studies on the conservation of rare plants have addressed population genetic structure and relationships between genetic variation and population size. Though important, these studies are not suitable for assessing the importance of genetics for population viability. In turn, demographic studies can detect changes in vital rates in small populations, but cannot reveal underlying genetic causes. Fitness and demographic studies are also well-represented in the literature, but remarkably few studies have attempted to integrate empirical demographic and genetic studies. We discuss two approaches to fill this very important lacuna in our knowledge. One of these constructs matrix-projection models on the basis of demographic censuses of—if possible—large and viable populations, and combines these with the results of experiments to determine inbreeding effects on demographic transitions and, subsequently, population growth and extinction. The other approach is to demographically monitor experimentally created small and large populations with low and high genetic variation and measure their actual growth rates and probabilities of extinction. We conclude that demography and demographic-genetic experiments should play a central role in plant conservation genetics.     

Local extinctions of the wetland specialist Swertia perennis L. (Gentianaceae) in Switzerland: a revisitation study based on herbarium records

We studied population extinction of the locally abundant fen plant Swertia perennis in Switzerland and used up to 127-year old herbarium records to relocate 63 sites that had once hosted this species. We recorded current site characteristics and related them to the absence or abundance of populations. Fifty-four sites (86%) were still traditionally used (extensively mown or grazed). Fifteen populations (24%) had gone extinct. Extinction was more likely at lower altitude, in the peripheral distribution range of S. perennis (58% peripheral, 9% central populations extinct), on the smallest fens (75% extinct on fens <400 m²) and on fens with intensified land use. However, even on traditionally managed wetlands 18.5% of the populations had gone extinct. Moreover, 40% of all remaining populations were smaller than 250 flowering plants. We conclude that both intensified agricultural practice and habitat fragmentation contributed to local extinction of S. perennis. Small populations, especially, may not be able to persist in the long term.     

Population demography and fecundity do not decline with habitat fragmentation in the rainforest tree Macadamia integrifolia (Proteaceae)

Habitat fragmentation is often associated with reduced levels of fitness and local extinction of plant species, and consequently poses a major threat to the persistence of species worldwide. The majority of demography-based fragmentation studies to date have focussed primarily on fragmentation impacts on individual plant fecundity. Here we investigate the impact of habitat fragmentation on the demography (plant height classes and density) and key population dynamic processes for the rainforest tree species Macadamia integrifolia (Proteaceae). Raceme and fruit production and seedling emergence across fragmented sites exceeded that in more intact sites with no apparent difference in short-term mortality rates. Fecundity of flowering trees did not appear to be affected by fragmentation. Instead, overall reproductive output in fragmented sites was enhanced relative to undisturbed sites due to a higher proportion of reproductively active individuals. The probability of flowering and fruiting was negatively correlated with the projected foliage cover (PFC) surrounding individual trees, and average PFC was significantly lower in small and medium fragments, suggesting light availability as a potential contributor to the trends observed here.This study demonstrates that the short-term effects of habitat fragmentation on population viability may not necessarily be detrimental for some species, and highlights the importance of assessing not only the fecundity of flowering individuals but also the proportion of individuals reproducing within fragments.     

Genetics of a butterfly relocation: large, small and introduced populations of the mountain endemic Erebia epiphron silesiana

Species specific levels of genetic diversity are necessary for the viability of populations. Erebia epiphron (Lepidoptera: Satyrinae) is a relic species in the Sudetan Mountains, Czech Republic. These populations represent a suitable study object to test the population genetic effects of large, small and introduced populations by means of allozyme electrophoresis. A large continuous and viable population (>100,000 individuals) shows a significantly higher genetic diversity than a small isolated and declining population (ca. 5000 individuals), which most probably was founded during the Little Ice Age in the 17th and 18th centuries and became isolated afterwards. In 1932 and 1933, 50 females were transferred from the large population to the Krkonose Mountains, where they established a viable and quickly expanding population. The number of transferred individuals was sufficient to transfer most of the allozyme diversity of the large natural population. Due to the higher elevation of the Krkonose in comparison to the native range, this allocation might safeguard the survival of the Czech race of E. epiphron even under conditions of global warming.     

Demographic effects of road mortality in black ratsnakes (Elaphe obsoleta)

Roads negatively affect animal populations by presenting barriers to movement and gene flow and by causing mortality. We investigated the impact of a secondary road on a population of black ratsnakes (Elaphe obsoleta) in Ontario, Canada by radio-tracking 105 individuals over 8 years. The road was not a significant barrier to movement and none of the reproductive classes examined (male, non-reproductive female, reproductive female) avoided crossing the road. However, the road was a significant source of mortality. From a total of 115 road crossings by radio-implanted snakes, 3 individuals were killed by cars, resulting in a mortality rate of 0.026 deaths per crossing. We multiplied this mortality rate by the total number of expected road crossings by all individuals in the population in an active season (340) to estimate the number of road kills (9 individuals) each year. This estimate was higher than the actual number of road kills found, but half the number estimated from road kill models. Population viability analysis revealed that our estimate of road mortality was enough to increase the extinction probability for this population from 7.3% to 99% over 500 years. Road mortality of more than 3 adult females per year increased the extinction probability to >90%. Our results strengthen the view that road mortality can have a pronounced negative effect on populations of long-lived species.     

Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates

Population size is a major determinant of extinction risk. However, controversy remains as to how large populations need to be to ensure persistence. It is generally believed that minimum viable population sizes (MVPs) would be highly specific, depending on the environmental and life history characteristics of the species. We used population viability analysis to estimate MVPs for 102 species. We define a minimum viable population size as one with a 99% probability of persistence for 40 generations. The models are comprehensive and include age-structure, catastrophes, demographic stochasticity, environmental stochasticity, and inbreeding depression. The mean and median estimates of MVP were 7316 and 5816 adults, respectively. This is slightly larger than, but in general agreement with, previous estimates of MVP. MVPs did not differ significantly among major taxa, or with latitude or trophic level, but were negatively correlated with population growth rate and positively correlated with the length of the study used to parameterize the model. A doubling of study duration increased the estimated MVP by approximately 67%. The increase in extinction risk is associated with greater temporal variation in population size for models built from longer data sets. Short-term studies consistently underestimate the true variances for demographic parameters in populations. Thus, the lack of long-term studies for endangered species leads to widespread underestimation of extinction risk. The results of our simulations suggest that conservation programs, for wild populations, need to be designed to conserve habitat capable of supporting approximately 7000 adult vertebrates in order to ensure long-term persistence.     

Evaluation of the extinction risk and of conservation alternatives for a very small insular population: the bearded vulture Gypaetus barbatus in Corsica

The bearded vulture Gypaetus barbatus is a large, long-lived osteophagus vulture whose abundance and breeding range have drastically declined during the last century, making it one of the most endangered European bird species. We evaluated the extinction risk of the bearded vulture population in Corsica (a small, isolated breeding population of 8-10 pairs), one of the last extant populations in Western Europe, and estimated its probability of extinction to be 0.165 over the next 50 years. A sensitivity analysis to assess the influence of uncertain demographic rates showed that it is critical to estimate precisely the values of pre-adult survival. Neither the type nor the parameters of density dependence acting on fecundity and survival rates influenced much the extinction risk of the Corsican population. We evaluated the effect of four realistic conservation actions that could be implemented on the Corsican bearded vulture population and rank them in terms of their respective decrease of the current extinction risk faced by this population. We found that the release of two juveniles every other year for 12 years and the increase of fecundity due to selective food provisioning would reduce by more than one-half the current extinction risk of Corsican bearded vulture population. In contrast, even substantial increases in the carrying capacity through large supplemental feeding produced very modest decreases in the extinction risk, thus calling into question the efficacy of one of the main pan-European conservation strategies for this species. Re-establishing a population network within the Mediterranean could be a potentially better strategy, though its efficacy depends on natal dispersal among populations that is currently unknown.     

Metapopulation dynamics and conservation of the marsh fritillary butterfly: Population viability analysis and management options for a critically endangered species in Western Europe

This study investigates the dynamics and viability of a marsh fritillary butterfly Euphydryas aurinia metapopulation in a Belgian successional landscape. Based on capture-mark-recapture and winter nest census data, we first estimated demography (survival and recruitment rates, population size, density dependence) and dispersal parameters (emigration rate, effect of patch connectivity on dispersal, mortality during dispersal). Then using RAMAS/GIS platform, we parameterised a population viability analysis (PVA) model with these parameters to simulate the future of this metapopulation under different scenarios.The metapopulation does not seem viable even if natural reforestation is controlled by adequate management. In its present state, the patch system is not able to sustain enough individuals: due to the large temporal fluctuations in demographic parameters, a carrying capacity far higher than currently would be necessary to limit extinction risk to 1%, suggesting the existence of an extinction debt for the species in Belgium. The situation of E. aurinia appears much worse compared to two other fritillary species threatened in Belgium, for which similar PVA are available. It is therefore urgent to increase the carrying capacity of the patch system. How and where it is achieved are of secondary importance for the gain in viability: improvement of habitat quality through restoration, or increase of habitat quantity via enlargement of existing patches and/or creation of new habitat in the matrix. A regime of management based on regular re-opening and maintenance of habitat patches may be the only guarantee of long-term persistence for this critically endangered species in Belgium.     

Inbreeding in red-cockaded woodpeckers: Effects of natal dispersal distance and territory location

Inbreeding depression constitutes a significant threat to the viability of small populations. In addition to small size and isolation of populations, short distance dispersal may elevate risk of inbreeding, but empirical evidence is scarce. Inbreeding depression has been demonstrated in the highly endangered red-cockaded woodpecker Picoides borealis. It has been suggested that conservation efforts to support extant populations should aim at spatially aggregating territories to enhance dispersal success. This however may aggravate inbreeding risk because distance between territories and hence dispersal distances become short. We analysed empirical data from a long-term study of the demography of the red-cockaded woodpecker and found that inbreeding risk varied inversely with natal dispersal distance of the mother. Using an individual-based, spatially explicit population model that incorporates simulations of environmental and demographic stochasticity and an empirically derived, species-specific estimate of inbreeding costs, we demonstrated that inbreeding depression significantly elevated extinction risk in this species. On the other hand, even though dispersal distances in populations with spatially aggregated territories were shorter and the proportion of inbred individuals was higher than in other populations of the same size, such populations were still more persistent. Despite the overall adverse effect of inbreeding depression on viability of red-cockaded woodpecker populations, lowering interterritorial distances can be viewed as a valuable conservation tool. Given the small size and isolated location of most extant red-cockaded woodpecker populations however, our findings suggest that inbreeding depression represents a significant threat to the survival of this species.     

Evaluating population persistence of Delmarva fox squirrels and potential impacts of climate change

In addition to the combined effects of forest fragmentation, habitat loss, and population isolation on the long-term persistence of many species including the endangered Delmarva fox squirrel (Sciurus niger cinereus), future changes in climate may make existing habitats less productive and more variable. The Palmer Drought Severity Index (PDSI) for the Delmarva Peninsula of the mid-Atlantic USA, reveals a trend for longer durations of potentially unfavorable conditions for fox squirrel population growth. We used a stochastic population matrix model and available life history information to assess population extinction risk for the Delmarva fox squirrel under a number of scenarios of landscape change and environmental variation, including uncertainties in the future range of climate patterns. Patch size (carrying capacity) was the most important factor influencing persistence of isolated populations. Extinction risk increased markedly across all patch sizes when year to year patterns in environmental variability were autocorrelated to match regional patterns in the PDSI. Increased autocorrelation matching the regional PSDI increased extinction risk, ranging from a factor of 5 to a factor of over 100 in some scenarios when compared to uncorrelated patterns in environmental variability. Increasing the range of variation in survival probabilities was less important to persistence, but its effect also increased when year-to-year changes were autocorrelated in time. Comparing model results with the size and landscape configuration of currently occupied patches on the Delmarva Peninsula showed that many existing populations are above the size threshold identified by these simulations for long-term persistence under current conditions, but these may become vulnerable should climate variability increase and adverse conditions persist for several years at a time.     

Is the collection of Aloe peglerae from the wild sustainable? An evaluation using stochastic population modelling

Aloe peglerae Schönland, an Endangered species endemic to South Africa, is threatened mainly by illegal collection. Lower densities of plants in areas easily accessible to the public led to questions concerning the sensitivity of this species to collection. Demographic monitoring data collected between 1976 and 1995 were used to build a stochastic population model, where parameters were allowed to vary randomly between observed minimum and maximum values. The model indicated that A. peglerae is highly sensitive to harvest of adult plants, with use sustainable at only very low levels of not more than 0.12%. Harvesting one plant annually is only sustainable in large populations of more than 1000 individuals; populations of this size, however, are rare. A maximum of fifteen percent of the annual seed output can be harvested sustainably. This long-term evaluation demonstrates that current collection of this species from the wild is unsustainable. Ex situ cultivation is therefore vital.     

Winter flocking behaviour of speckled warblers and the Allee effect

The aggregation of individuals into foraging flocks is one behavioural trait that, if disrupted, can cause the Allee effect, which is a slowing in population growth at low density or small population size, and this can greatly increase the risk of extinction. Here, I describe intraspecific flocking behaviour of a colour-banded population of speckled warblers, Chthonicola sagittata, a species that has declined across a large part of its range in the fragmented temperate woodlands of Australia. I make predictions about the context in which the Allee effect might be expressed and the consequences for the viability of populations living in small habitat remnants. Speckled warblers lived in discrete, stable social groups throughout winter, the nucleus of which was the residents from one or more adjacent breeding territories. The timing and mode of flock formation and the size of flocks varied between two winters, apparently in response to the severity of conditions; thus flocking probably facilitates increased foraging efficiency and predator detection, potentially leading to increased survival in harsh conditions. Because flock territories were up to 30 ha each, and larger territories are likely, birds living in remnants smaller than 40 ha may suffer increased mortality if there are too few birds available to form flocks of an appropriate size to facilitate the benefits of grouping when conditions are most extreme. Further, in small remnants where survival is reduced, dominance behaviour and male-male competition may act to compound the Allee effect by reducing reproductive success. Regardless of these predictions, speckled warbler populations may only be viable in remnants that are large enough to support multiple flocks, to enable rapid recruitment to breeding vacancies and thus provide adequate numbers of birds for flocking.     

Probable consequences of high female mortality for speckled warblers living in habitat remnants

The effects of habitat fragmentation on the Australian avifauna have been widespread with species richness and abundance declining with reduced remnant size and habitat quality and increased habitat isolation. The speckled warbler, Chthonicola sagittata is one species from the highly fragmented temperate woodlands of eastern Australia that has declined across its range and populations that remain appear to be patchily distributed in habitat remnants. Specific causes of decline are unknown but several aspects of its biology make the species particularly vulnerable to decline in fragmented landscapes. Here, we analyse survey data (presence/absence) of speckled warblers in a large sample of habitat remnants from three regions to identify patterns of occupancy. We explore the effects of patch size on extinction risk using population viability analyses (PVA) and detailed demographic data from a behavioural study of individuals in the Australian Capital Territory, south-eastern Australia. Patch size was a strong predictor of the persistence of speckled warblers in habitat remnants. High density populations had higher probabilities of persisting, and inclusion of an Allee effect during drought decreased the probability of persistence. In the absence of an Allee effect, only high density populations in patches greater than 300 ha and low density populations in patches greater than700 ha had more than an 80% probability of persisting over 100 years. The accelerating decrease in population persistence below approximately 200-400 ha suggests that small populations were particularly vulnerable to stochastic demographic and environmental events. Adult female mortality was the single most important factor in driving population extinction. Our PVA model predictions matched the survey data for the Australian Capital Territory region remarkably well, but failed to predict occupancy rates in remnants in other regions. Differences in occupancy patterns between regions may, however, have resulted from inbreeding depression. This study demonstrates both the strengths and limitations of PVA analysis. PVA can predict occupancy patterns with reasonable accuracy, given good demographic data, but data for one region cannot be used universally for all regions. We highlight the need for studies of demography in different regions to interpret regional patterns of occupancy and to identify mechanisms of decline in remnant habitat.