Continental‐scale determinants of population trends in European amphibians and reptiles

The continuous decline of biodiversity is determined by the complex and joint effects of multiple environmental drivers. Still, a large part of past global change studies reporting and explaining biodiversity trends have focused on a single driver. Therefore, we are often unable to attribute biodiversity changes to different drivers, since a multivariable design is required to disentangle joint effects and interactions. In this work, we used a meta‐regression within a Bayesian framework to analyze 843 time series of population abundance from 17 European amphibian and reptile species over the last 45 years. We investigated the relative effects of climate change, alien species, habitat availability, and habitat change in driving trends of population abundance over time, and evaluated how the importance of these factors differs across species. A large number of populations (54%) declined, but differences between species were strong, with some species showing positive trends. Populations declined more often in areas with a high number of alien species, and in areas where climate change has caused loss of suitability. Habitat features showed small variation over the last 25 years, with an average loss of suitable habitat of 0.1%/year per population. Still, a strong interaction between habitat availability and the richness of alien species indicated that the negative impact of alien species was particularly strong for populations living in landscapes with less suitable habitat. Furthermore, when excluding the two commonest species, habitat loss was the main correlate of negative population trends for the remaining species. By analyzing trends for multiple species across a broad spatial scale, we identify alien species, climate change, and habitat changes as the major drivers of European amphibian and reptile decline.     

Can the introduction of Xenopus laevis affect native amphibian populations? Reduction of reproductive occurrence in presence of the invasive species

Biological invasions are regarded as a form of global change and potential cause of biodiversity loss. Xenopus laevis is an anuran amphibian native to sub-Saharan Africa with strong invasive capacity, especially in geographic regions with a Mediterranean climate. In spite of the worldwide diffusion of X. laevis, the effective impact on local ecosystems and native amphibian populations is poorly quantified. A large population of X. laevis occurs in Sicily and our main aim of this work was to assess the consequences of introduction of this alien species on local amphibian populations. In this study we compare the occurrence of reproduction of native amphibians in ponds with and without X. laevis, and before and after the alien colonization. The results of our study shows that, when X. laevis establishes a conspicuous population in a pond system, the populations of Discoglossus pictus, Hyla intermedia and Pelophylax synklepton esculentus show clear signs of distress and the occurrence of reproduction of these native amphibians collapses. In contrast, the populations of Bufo bufo do not appear to be affected by the alien species. Since the Sicilian population of X. laevis shows a strong dispersal capacity, proportionate and quick interventions become necessary to bound the detriment to the Sicilian amphibians populations.     

Comparison of susceptibility to a toxic alien toad (Bufo japonicus formosus) between predators in its native and invaded ranges

1. To manage biological invasions effectively, the impacts of alien species on the demography and traits of native species must be known, but determining those impacts can be challenging. We used a comparative approach to gain insight into the impacts that an alien toad (Bufo japonicus formosus) might have on native Japanese predatory amphibians. We compared the susceptibility of native predator species to alien toad toxins in the alien-invaded range and the susceptibility of closely related native predator species to the toxins in the alien toad's native range to investigate the impacts of an alien on a native species.
2. Bufo japonicus formosus is native to Honshu, but was recently introduced to Hokkaido and Sado. In laboratory experiments, we compared individual mortality of predators exposed to a toad hatchling between novel predators on the toad-invaded islands and ecologically similar congeneric or conspecific species on Honshu, where the toad is native. We also compared (1) the percentage of individuals that consumed a toad hatchling and (2) toxin resistance (i.e. survival and growth of individuals after toad consumption) between these two groups of predators, as mechanistic components behind the susceptibility of the predators to the toxic prey.
3. The mortality of Rana pirica from all populations after consumption of a toad hatchling was almost 100%, and that of Hynobius retardatus ranged from 14 to 90%, depending on the population. In contrast, the mortality of Rana ornativentris and Hynobius nigrescens was near 0% regardless of population. These differences between congeneric predators were mostly due to differences in their toxin resistance.
4. These results suggest that the alien toad is a potential threat to the novel amphibian predators on Hokkaido, although they also imply that the novel predators on Hokkaido have the potential to develop toxin resistance through adaptive evolution. However, this counteradaptation may have a higher chance of evolving in H. retardatus than in R. pirica because of differences in their genetic backgrounds.

     

Alien predators are more dangerous than native predators to prey populations

Alien predators are widely considered to be more harmful to prey populations than native predators. To evaluate this expectation, we conducted a meta-analysis of the responses of vertebrate prey in 45 replicated and 35 unreplicated field experiments in which the population densities of mammalian and avian predators had been manipulated. Our results showed that predator origin (native versus alien) had a highly significant effect on prey responses, with alien predators having an impact double that of native predators. Also the interaction between location (mainland versus island) and predator origin was significant, revealing the strongest effects with alien predators in mainland areas. Although both these results were mainly influenced by the huge impact of alien predators on the Australian mainland compared with their impact elsewhere, the results demonstrate that introduced predators can impose more intense suppression on remnant populations of native species and hold them further from their predator-free densities than do native predators preying upon coexisting prey.     

Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?

Biological invasions are ecologically and economically costly. Understanding the major mechanisms that contribute to an alien species becoming invasive is seen as essential for limiting the effects of invasive alien species. However, there are a number of fundamental questions that need addressing such as why some communities are more vulnerable to invasion than others and, indeed, why some alien species become widespread and abundant. The enemy release hypothesis (ERH) is widely evoked to explain the establishment and proliferation of an alien species. ERH predicts that an alien species introduced to a new region should experience a decrease in regulation by natural enemies which will lead to an increase in the distribution and abundance of the alien species. At the centre of this theory is the assumption that natural enemies are important regulators of populations. Additionally, the theory implies that such natural enemies have a stronger regulatory effect on native species than they do on alien species in the introduced range, and this disparity in enemy regulation results in increased population growth of the alien species. However, empirical evidence for the role of the ERH in invasion success is lacking, particularly for invertebrates. Many studies equate a reduction in the number of natural enemies associated with an alien species to release without studying population effects. Further insight is required in relation to the effects of specific natural enemies on alien and native species (particularly their ability to regulate populations). We review the role of ecological models in exploring ERH. We suggest that recent developments in molecular technologies offer considerable promise for investigating ERH in a community context.     

Risk induced by a native top predator reduces alien mink movements

1. Nonlethal predation effects may have stronger impacts on prey populations than direct predation impacts, and this should also apply to intraguild predation. The consequences of such interactions become especially important if invasive, and potentially destructive alien predators act as intraguild prey. 2. We studied the predation-risk impacts of a re-colonizing native top predator, Haliaeetus albicilla (white-tailed sea eagle), on the movements of Mustela vison (American mink), an alien predator in Europe. We radiocollared 20 mink in two study areas in the outer archipelago of the Baltic Sea, South-west Finland, during 2004 and 2005. In the archipelago, mink home ranges incorporate many islands, and mink are most predisposed to eagle predation while swimming between islands. Observed swimming distances of mink were compared to distances expected at random, and deviations from random swimming were explained by mink distance from nearest eagle nest, number of eagle observations near mink location, and mink home-range size. 3. Mink reduced their swimming distances with increasing sea eagle predation risk: for females, the reduction was 10% for an increase of 10 eagle observations, and 5% for each kilometre towards an eagle nest. Conclusions for males were restricted by their small sample size. 4. Our results suggest that female mink modify their behaviour according to eagle predation risk, which may reduce their population growth and have long-term cascading effects on lower trophic levels including bird, mammal and amphibian populations in the archipelago. Ecosystem restoration by bringing back the top predators may be one way of mitigating alien predator effects on native biota.     

两栖类种群数量下降原因及保护对策

近几十年来 ,全球范围内的两栖类出现了较快的种群数量下降 ,包括部分物种的灭绝。引起两栖类种群数量下降的原因可能有 :紫外线辐射、生境破碎和改变、生物入侵和捕食、环境污染、疾病、气候变化以及这些因素的相互作用 ,其中生境破碎和改变是主要原因 ,而引起各因素变化的全球变化可能是根本原因。应加强对两栖类种群动态的研究 ,探明其下降机制 ,制定相应的保护对策 ,减少两栖类的下降     

Effects of mammalian predators on partridge populations

Many ecologists have argued that predation is of little consequence in the regulation of gamebird numbers and that predator control in game management is a waste of time. Their case has included two lines of evidence; firstly, gamekeepers do not appear to be reducing predator numbers significantly; secondly, mortality by predation appears to be compensatory and therefore has little impact on gamebird populations as a whole. However, a closer examination of the activities of gamekeepers indicates that they do reduce predation pressure either by reducing or completely removing some predator species, or by temporarily reducing their number on a local basis. Recent research including an investigation of partridge population processes explored with a computer simulation model indicates that predation does regulate both autumn and spring densities. Other factors play an important role only when predators are removed.     

Predator-prey interactions in a nonequilibrium context: the metapopulation approach to modeling "hide-and-seek" dynamics in a spatially explicit tri-trophic system

Predators and prey are usually heterogeneously distributed in space so that the ability of the predators to respond to the distribution of their prey may have a profound influence on the stability and persistence of a predator‐prey system. A special type of dynamics is “hide‐and‐seek” characterized by a high turnover rate of local populations of prey and predators, because once the predators have found a patch of prey they quickly overexploit it, whereupon the starving predators either should move to better places or die. Continued persistence of prey and predators thus hinges on a long‐term balance between local extinctions and founding of new subpopulations. The colonization rate depends on the rate of emigration from occupied patches and the likelihood of successfully arriving at a suitable new patch, while extinction rate depends on the local population dynamics. Since extinctions and colonizations are both discrete probabilistic events, these phenomena are most adequately modeled by means of a stochastic model. In order to demonstrate the qualitative differences between a deterministic and stochastic approach to population dynamics, a spatially explicit tritrophic predator‐prey model is developed in a deterministic and a stochastic version. The model is parameterized using data for the two‐spotted spider mite (Tetranychus urticae) and the phytoseiid mite predator Phytoseiulus persimilis inhabiting greenhouse cucumbers.
Simulations show that the deterministic and stochastic approaches yield different results. The deterministic version predicts that the populations will exhibit violent fluctuations, implying that the system is fundamentally unstable. In contrast, the stochastic version predicts that the two species will be able to coexist in spite of frequent local extinctions of both species, provided the system consists of a sufficiently large number of local populations. This finding is in agreement with experimental results. It is therefore concluded that demographic stochasticity in combination with dispersal is capable of producing and maintaining sufficient asynchrony between local populations to ensure long‐term regional (metapopulation) persistence.     

Sport Hunting,Predator Control and Conservation of Large Carnivores

Sport hunting has provided important economic incentives for conserving large predators since the early 1970''s, but wildlife managers also face substantial pressure to reduce depredation. Sport hunting is an inherently risky strategy for controlling predators as carnivore populations are difficult to monitor and some species show a propensity for infanticide that is exacerbated by removing adult males. Simulation models predict population declines from even moderate levels of hunting in infanticidal species, and harvest data suggest that African countries and U.S. states with the highest intensity of sport hunting have shown the steepest population declines in African lions and cougars over the past 25 yrs. Similar effects in African leopards may have been masked by mesopredator release owing to declines in sympatric lion populations, whereas there is no evidence of overhunting in non-infanticidal populations of American black bears. Effective conservation of these animals will require new harvest strategies and improved monitoring to counter demands for predator control by livestock producers and local communities.     

Habitat-mediated impact of alien mink predation on common frog densities in the outer archipelago of the Baltic Sea

Alien predators have been recognised as one possible cause for amphibian declines around the world, but little is known of habitat-mediated predation impacts especially on adult amphibians. We studied common frog Rana temporaria under American mink Mustela vison predation in the outer archipelago of the Baltic Sea, south-western Finland. Using egg batches as an index of breeding frog female numbers we compared frog numbers and densities between a large, long-term mink-removal area and a comparable control area. Frog numbers in the removal area were at least 2.7-fold higher than those in the control area. In the presence of mink, frog densities increased with the amount of vegetation cover on the islands, indicating that mink predation affected frog densities especially on less-vegetated islands. An opposite trend appeared to be true for frogs in the mink-removal area, where other predators like snakes could induce a decline of frog densities on more vegetated islands. Shrub or grass vegetation seems to provide frogs shelter against alien mink predation. Our result highlights the importance of landscape-level habitat management as a conservation tool for amphibian populations.     

Can predators regulate wild Rabbit Oryctolagus cuniculus population density in England and Wales?

Predation has usually been interpreted as being a compensatory mortality factor, removing only the doomed surplus. The literature on the wild Rabbit Oryctolagus cuniculus L. is reviewed to collate counter-evidence for a regulating influence of predation. This evidence is almost entirely circumstantial, not experimental. Predation has been reported to extend the length of time Rabbit populations remain low following a significant reduction of Rabbits by some other agent. Rabbit populations have been shown to increase very rapidly when predator density has suddenly been reduced. It has been suggested that predators affect the spread and dispersion of Rabbits both at the geographical and local levels. Predation has not, however, been shown to have an important influence at high Rabbit densities. Thus, its role can be that of a limiting factor rather than a density-dependent regulatory mortality factor. The concept of predator pressure is presented and discussed, pointing out that there is currently no standard technique used for its measurement. Further evidence on the importance of predation is presented from four recent studies in England and Wales that relate, by association, the distribution and abundance of local Rabbit populations to the local attitude towards predators. Rabbits were found to be significantly more widespread and abundant where predators were removed (not restricted to keepered game estates) or at low density, than when predators were undisturbed or at a high density. The significance of these results is discussed. The circumstantial and corroborative evidence leads strongly to the conclusion that predator pressure can act as an additive rather than compensatory mortality factor in some circumstances, and can thus be a potential regulating factor. Predation is more likely to be a limiting factor at low Rabbit density however, since a density-dependent relationship has not been demonstrated throughout the range of Rabbit densities that occur. This requires experimental demonstration to determine the threshold pressure below which predation becomes limiting. If so, reductions in Rabbit populations by short-term control operations could allow natural predation to help maintain low Rabbit densities for several years in some habitats. Conversely, the implications for Rabbit populations and thus crop damage resulting from predator control (e.g. in game management regimes) should be appreciated.     

Experimental and observational evidence reveals that predators in natural environments do not regulate their prey: They are passengers,not drivers

Among both ecologists and the wider community there is a tacit assumption that predators regulate populations of their prey. But there is evidence from a wide taxonomic and geographic range of studies that predators that are adapted to co-evolved prey generally do not regulate their prey. This is because predators either cannot reproduce as fast as their prey and/or are inefficient hunters unable to catch enough prey to sustain maximum reproduction. The greater capacity of herbivores to breed successfully is, however, normally restricted by a lack of enough food of sufficient quality to support reproduction. But whenever this shortage is alleviated by a large pulse of food, herbivores increase their numbers to outbreak levels. Their predators are unable to contain this increase, but their numbers, too, surge in response to this increase in food. Eventually both their populations will crash once the food supply runs out, first for the herbivores and then for the predators. Then an “over-run” of predators will further depress the already declining prey population, appearing to be controlling its abundance. This latter phenomenon has led many ecologists to conclude that predators are regulating the numbers of their prey. However, it is the same process that is revealed during outbreaks that limits populations of both predator and prey in “normal” times, although this is usually not readily apparent. Nevertheless, as all the diverse cases discussed here attest, the abundance of predators and their co-evolved prey are both limited by their food: the predators are passengers, not drivers.     

Attendance to egg clutches by male Kurixalus eiffingeri increases hatching success and decreases predation by invasive slugs (Parmarion martensi) in Taiwan

Invasive species have a significant impact on amphibians, and most notably Chytrid fungi together with a few vertebrates. However, invasive terrestrial invertebrates are seldomly demonstrated to have a negative effect on their host environment, and few studies investigated the behavioural interactions between invasive and local species, limiting our knowledge of the adaptive response adopted by local organisms. These responses include whether parenting animals recognize predators as threats to their offspring and whether parental care is adequately corrected. Here, through manipulative experiments on a population of phytotelm‐breeder Kurixalus eiffingeri in central Taiwan, we demonstrated the positive effects of parental care against predation by the invasive slug Parmarion martensi, and against mould infection. Treatment groups, in the absence of caring males, displayed a higher rate of predation by slugs and mould infections. The presence of the caring males was linked to an increase in hatching success in control groups, suggesting hydration by the males, while skin peptides may be the factor limiting mould infection. We recommend further research on the impact of the invasive but widespread P. martensi on amphibian populations.     

Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations?

Amphibians are frequently characterized as having limited dispersal abilities, strong site fidelity and spatially disjunct breeding habitat. As such, pond‐breeding species are often alleged to form metapopulations. Amphibian species worldwide appear to be suffering population level declines caused, at least in part, by the degradation and fragmentation of habitat and the intervening areas between habitat patches. If the simplification of amphibians occupying metapopulations is accurate, then a regionally based conservation strategy, informed by metapopulation theory, is a powerful tool to estimate the isolation and extinction risk of ponds or populations. However, to date no attempt to assess the class‐wide generalization of amphibian populations as metapopulations has been made. We reviewed the literature on amphibians as metapopulations (53 journal articles or theses) and amphibian dispersal (166 journal articles or theses for 53 anuran species and 37 salamander species) to evaluate whether the conditions for metapopulation structure had been tested, whether pond isolation was based only on the assumption of limited dispersal, and whether amphibian dispersal was uniformly limited. We found that in the majority of cases (74%) the assumptions of the metapopulation paradigm were not tested. Breeding patch isolation via limited dispersal and/or strong site fidelity was the most frequently implicated or tested metapopulation condition, however we found strong evidence that amphibian dispersal is not as uniformly limited as is often thought. The frequency distribution of maximum movements for anurans and salamanders was well described by an inverse power law. This relationship predicts that distances beneath 11–13 and 8–9 km, respectively, are in a range that they may receive one emigrating individual. Populations isolated by distances approaching this range are perhaps more likely to exhibit metapopulation structure than less isolated populations. Those studies that covered larger areas also tended to report longer maximum movement distances – a pattern with implications for the design of mark‐recapture studies. Caution should be exercised in the application of the metapopulation approach to amphibian population conservation. Some amphibian populations are structured as metapopulations – but not all.     

Amphibian declines: future directions

Abstract. The amphibian decline problem is complex, and there is no easy solution. I highlight four major areas of future research that should increase our ability to detect declines, elucidate their underlying mechanisms, and advance our capacity to manage and conserve amphibian populations. First, a statistically sensitive monitoring approach is necessary to determine the distribution and abundance of amphibian populations, to assess whether they are declining, and to quantify the extent of declines. Most amphibian populations characteristically fluctuate, detection probabilities may be low for many species and populations tend to decline in numbers between years more often than they increase. These traits make establishing monitoring programmes difficult and distinguishing declines from natural fluctuations challenging. It is thus necessary to determine the best monitoring techniques based on their statistical power and to use appropriate statistical methods for detecting population trends. Secondly, although amphibian population studies occur most commonly at single or few breeding sites, research should occur often at the landscape level, and conservation efforts should focus on suitable habitat (whether or not it is occupied) and dispersal capabilities of species. Metapopulation dynamics are probably important for many species, but we must be cautious how we define metapopulations. That is, the term ‘metapopulation’ is currently used to define a wide range of demographic situations in amphibian populations, each with different management implications. Thirdly, recent advances in molecular genetic techniques make it possible to infer demographic events such as effects of recent fragmentation, bottlenecks or hybridization. Molecular techniques can be used in conjunction with census surveys to bolster knowledge about demographic processes such as declines. Alternatively, in the absence of long‐term census data, molecular data can be used to infer population trends. New genomic approaches may make estimating adaptive genetic variation more feasible. Fourthly, multi‐factorial studies are needed to disentangle the complexity of the several putative causes that probably interact to cause amphibian declines. Recent studies demonstrate the value of a multi‐factorial approach, and more work is needed to elucidate the synergistic effects of multiple environmental factors affecting amphibian populations simultaneously worldwide.     

The influence of landscape structure on occurrence, abundance and genetic diversity of the common frog, Rana temporaria

Human‐caused habitat destruction and modification constitute one of the largest threats to population persistence and biodiversity, and are also suspected to be the major cause behind the global decline of amphibian populations. We assessed the potential role of agriculture‐related habitat fragmentation on population size and genetic variability in the common frog (Rana temporaria) by recording the occurrence, population density and genetic diversity in three geographically disparate regions in Sweden – each containing landscapes of high and low agricultural activity – and related these to landscape variables extracted from digital maps. We found a highly significant region‐by‐landscape interaction in occurrence, population density and genetic diversity revealing a reversed response to agriculture from south to north: while the effects of agriculture on R. temporaria populations were negative in the south, there were no effects in the central region, whereas positive effects were observed in the north. Spatial autocorrelation analyses of genetic data revealed that populations in high agricultural activity areas were more isolated than populations in low activity areas both in the southern and central regions of Sweden. Landscape diversity showed a strong positive correlation with both density and occurrence of frogs in Sweden as a whole, as well as in the southern region. Also, negative effects of roads and positive effects of ditches on genetic diversity were found in the south. Overall, these results suggest clear but regionally opposite effects of habitat structure on the population size and genetic diversity of amphibian populations. This means that the management strategy aiming to maximize the size and genetic diversity of local common frog populations, and perhaps also those of other amphibian populations, should account for regional differences in existing land‐use patterns.     

Assessing the potential impact of an invasive species on a Mediterranean amphibian assemblage: a morphological and ecological approach

The introduction of exotic species is a major cause of ecological disturbance and has recently been shown to promote the decline of some amphibian populations. In Western Europe, several amphibian species have been introduced in recent decades, among them Discoglossus pictus, impact of which in native amphibian communities is still unknown. We studied the potential impact of D. pictus by analysing the degree of niche overlap, assuming the possible existence of competitive interactions with native species. We have studied the structure of the anuran assemblage at local level, defining the morphospace occupied by native species and the habitat occupied by the different ecomorphs. The analysis of distance matrices suggested that there was a covariation between morphological characters and habitat selection. We determined the position of D. pictus within the morphospace of the native anuran community, patterns of co-occurrence among alien, and native species and habitat selection. The potential effect of climate on local assemblages had been controlled based on data obtained from climate models. These analysis showed that D. pictus was clustered with the benthic guild, selected positively small ephemeral ponds and was a thermophilic species. Based on these results, a greater degree of niche overlap was expected with Bufo calamita and Pelodytes punctatus. The definition of morphological groups can be useful to understand the invaded assemblage structure and the potential effect of an alien frog on native communities.     

Associations between Non‐Lethal Injury,Body Size,and Foraging Ecology in an Amphibian Intraguild Predator

Theoretical treatments of intraguild predation and its effects on behavioral interactions regard the phenomenon as a size‐structured binary response wherein predation among competitors is completely successful or completely unsuccessful. However, intermediate outcomes occur when individuals escape intraguild (IG) interactions with non‐lethal injuries. While the effects of wounds for prey include compromised mobility and increased predation risk, the consequences of similar injuries among top predators are not well understood, despite the implications for species interactions. Using an amphibian IG predator, Ambystoma opacum (Caudata: Ambystomatidae), we examined associations between non‐lethal injuries and predator body size, foraging strategy, microhabitat selection, and intraspecific agonistic interactions. Wounds were common among IG predators, generally increasing in frequency throughout larval ontogeny. Non‐lethal injuries were associated with differences in predator body size and behavior, with injured predators exhibiting smaller body sizes, increased use of benthic microhabitats, reduced agonistic displays, and increased risk of intraspecific aggression. While such effects were not ultimately associated with reduced foraging success, non‐lethal injury could contribute to niche partitioning between injured and healthy predators via habitat selection, but injured predators likely continue to exert predatory pressure on IG and basal prey populations. Our results indicate that studies of top‐down population regulation should incorporate injury‐related modifications to both prey and predator behavior and size structure.