Population Declines and Priorities for Amphibian Conservation in Latin America

Abstract: Although dramatic amphibian population declines have been reported worldwide, our understanding of the extent of the declines in Latin America, where amphibian diversity is high, is limited to a few well-documented studies. To better understand the geographic extent of declines, their possible causes, and the measures needed to improve Latin American scientists' ability to research the phenomenon and make effective management recommendations, we convened three regional workshops with 88 Latin American herpetologists and conservationists. Population declines are widespread in Latin America. At least 13 countries have experienced declines, and in 40 cases species are now thought to be extinct or extirpated in a country where they once occurred. Declines or extinctions have affected 30 genera and nine families of amphibians. Most declines have occurred in remote highlands, above 500 m in elevation in Central America and above 1000 m in the Andes. Most documented declines occurred in the 1980s. Of the possible causes studied to date, climate change appears to be important at one site and chytrid fungal disease has been identified at sites in three countries. Although many monitoring studies are currently underway in a variety of habitats, most studies are recent and of short duration. In a signed resolution, workshop participants called for greater collaboration and communication among scientists working in Latin America to understand the geographic extent of population declines and the distribution of possible causal factors. In situ conservation is important to protect habitats, but captive-rearing programs for species subject to imminent extinction are also needed. Better understanding of the taxonomy and natural history of amphibians and more funding for research and monitoring are critical to developing a scientific basis for management action to arrest and reverse population declines.     

Body Size and Risk of Extinction in Australian Mammals

Abstract: The link between body size and risk of extinction has been the focus of much recent attention. For Australian terrestrial mammals this link is of particular interest because it is widely believed that species in the intermediate size range of 35–5500 g (the "critical weight range") have been the most prone to recent extinction. But the relationship between body size and extinction risk in Australian mammals has never been subject to a robust statistical analysis. Using a combination of randomization tests and phylogenetic comparative analyses, we found that Australian mammal extinctions and declines have been nonrandom with respect to body size, but we reject the hypothesis of a critical weight range at intermediate sizes. Small species appear to be the least prone to extinction, but extinctions have not been significantly clustered around intermediate sizes. Our results suggest that hypotheses linking intermediate body size with high risk of extinction in Australian mammals are misguided and that the focus of future research should shift to explaining why the smallest species are the most resistant to extinction.     

Modern Insect Extinctions, the Neglected Majority

Abstract:  Most extinctions estimated to have occurred in the historical past, or predicted to occur in the future, are of insects. Despite this, the study of insect extinctions has been neglected. Only 70 modern insect extinctions have been documented, although thousands are estimated to have occurred. By focusing on some of the 70 documented extinctions as case studies, I considered ways in which insect extinctions may differ from those of other taxa. These case studies suggested that two types of extinction might be common for insects but rare for other taxa: extinction of narrow habitat specialists and coextinctions of affiliates with the extinctions of their hosts. Importantly, both of these forms of extinction are often ignored by conservation programs focused on vertebrates and plants. Anecdotal evidence and recent simulations suggest that many insect extinctions may have already occurred because of loss of narrow habitat specialists from restricted habitats and the loss of hosts. If we are serious about insect conservation, we need to spend more time and money documenting such extinctions. To neglect such extinctions is to ignore the majority of species that are or were in need of conservation.     

Demographic Processes Underlying Population Growth and Decline in Salamandra salamandra

Abstract:  Human activity commonly has negative impacts on wildlife. Often, however, only a single element of the life cycle is affected, and it is unclear whether such effects translate into effects on population growth. This is particularly true for research into the causes of global amphibian declines, where experimental research focuses primarily on the aquatic larval stages but theory suggests these stages have only minor importance for population growth. We used data from long-term mark-recapture studies of two natural populations of the salamander Salamandra salamandra to confirm the predictions of population models. One population remained stable (i.e., stationary) throughout the 20 years of the study whereas the other declined to local extinction. We used mark-recapture models to break down population growth rate into its two main components, recruitment and adult survival. Survival of postmetamorphic salamanders was constant over time in the stable population, whereas the declining population was characterized by a decrease in survival and constant recruitment. Population growth was most sensitive to variation in adult survival. Current amphibian research focuses on preadult stages, and researchers assume recruitment is the most important determinant of population growth. This may not be the case. A better understanding of amphibian population dynamics is possible only through the integration of experiments, theory, and data from natural populations. Our results also suggest that amphibian conservation efforts should focus on all stages of the life cycle and their associated habitats.     

Conserving the abundance of nonthreatened species

Human modification of the environment is driving declines in population size and distributional extent of much of the world's biota. These declines extend to many of the most abundant and widespread species, for which proportionally small declines can result in the loss of vast numbers of individuals, biomass, and interactions. These losses could have major localized effects on ecological and cultural processes and services without elevating a species’ global extinction risk. Although most conservation effort is directed at species threatened with extinction in the very near term, the value of retaining abundance regardless of global extinction risk is justifiable based on many biodiversity or ecosystem service metrics, including cultural services, at scales from local to global. The challenges of identifying conservation priorities for widespread and abundant species include quantifying the effects of species’ abundance on services and understanding how these effects are realized as populations decline. Negative effects of population declines may be disconnected from the threat processes driving declines because of species movements and environment flows (e.g., hydrology). Conservation prioritization for these species shares greater similarity with invasive species risk assessments than extinction risk assessments because of the importance of local context and per capita effects of abundance on other species. Because conservation priorities usually focus on preventing the extinction of threatened species, the rationale and objectives for incorporating declines of nonthreatened species must be clearly articulated, going beyond extinction risk to encompass the range of likely harmful effects (e.g., secondary extinctions, loss of ecosystem services) if declines persist or are not reversed. Research should focus on characterizing the effects of local declines in species that are not threatened globally across a range of ecosystem services and quantifying the spatial distribution of these effects through the distribution of abundance. The case for conserving abundance in nonthreatened species can be made most powerfully when the costs of losing this abundance are better understood.     

The Role of Behavior in Recent Avian Extinctions and Endangerments

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

Inconclusiveness of Chytridiomycosis as the Agent in Widespread Frog Declines

Abstract:  Although there is considerable evidence to support the hypothesis that the chytrid fungus Batrachochytrium dendrobatidis is the primary agent responsible for widespread declines in amphibian populations, particularly rainforest frog populations in Australia and Central America, I argue the case has not yet been made conclusively. Few specimens were collected at the time of population declines, so it may never be possible to conclusively determine their cause. It remains unclear whether the pathogen is novel where declines have occurred. Although it is not necessary that the infection be novel for it to be implicated in declines, if a preexisting pathogen has only recently caused extinctions, cofactors must be important. Whether the pattern of outbreaks represents a "wave" of extinctions is unclear, but if it does, the rate of spread in Australia is implausibly high for a waterborne pathogen, given the most likely estimates of epidemiological parameters. Although B. dendrobatidis is an amphibian pathogen according to Koch's postulates, the postulates are neither necessary nor sufficient criteria to identify a pathogen. The following key pieces of information are necessary to better understand the impact of this fungus on frog communities: better knowledge of the means and rate of transmission under field conditions, prevalence of infection among frog populations, as distinct from morbid individuals, and the effect of the fungus on frogs in the wild. It is crucial to determine whether there are strains of the fungus with differing pathogenicity to particular frog species and whether host-pathogen coevolution has occurred or is occurring. Recently developed diagnostic tools bring into reach the possibility of addressing these questions and thus developing appropriate strategies to manage frog communities that may be affected by this fungus.     

Extinction, Colonization, and Metapopulations: Environmental Tracking by Rare Species

Extinction and metapopulation theories emphasize that stochastic fluctuations in local populations cause extinction and that local extinctions generate empty habitat patches that are then available for recolonization. Metapopulation persistence depends on the balance of extinction and colonization in a static environment. For many rare and declining species, I argue (1) that extinction is usually the deterministic consequence of the local environment becoming unsuitable (through habitat loss or modification, introduction of a predator, etc.); (2) that the local environment usually remains unsuitable following local extinction, so extinctions only rarely generate empty patches of suitable habitat; and (3) that colonization usually follows improvement of the local environment for a particular species (or long-distance transfer by humans). Thus, persistence depends predominantly on whether organisms are able to track the shifting spatial mosaic of suitable environmental conditions or on maintainance of good conditions locally.     

Hypothesis Concerning the Causes of the Disappearance of Boreal Toads from the Mountains of Colorado

Recent reports of world-wide declines and extinctions of amphibian populations have raised questions about the relation of environmental change to the demise of certain amphibian species. Between 1974 and 1982, 11 populations of boreal toads ( Bufo boreas boreas ) in the West Elk Mountains of Colorado totally disappeared. The apparent cause of extinction of these toads was infection with the bacteria Aeromonas hydrophila . In this paper, the presence of disease in declining populations of these toads is used in conjunction with a variety of data from the literature to formulate a working hypothesis for explaining the cause of the decline of this species, and perhaps others:

     

Association of Coloration Mode with Population Declines and Endangerment in Australian Frogs

Abstract: Successful protection of biodiversity requires increased understanding of the ecological characteristics that predispose some species to endangerment. Theory posits that species with polymorphic or variable coloration should have larger distributions, use more diverse resources, and be less vulnerable to population declines and extinctions, compared with taxa that do not vary in color. We used information from literature on 194 species of Australian frogs to search for associations of coloration mode with ecological variables. In general, species with variable or polymorphic color patterns had larger ranges, used more habitats, were less prone to have a negative population trend, and were estimated as less vulnerable to extinction compared with nonvariable species. An association of variable coloration with lower endangerment was also evident when we controlled statistically for the effects of range size. Nonvariable coloration was not a strong predictor of endangerment, and information on several characteristics is needed to reliably identify and protect species that are prone to decline and may become threatened by extinction in the near future. Analyses based on phylogenetic‐independent contrasts did not support the hypothesis that evolutionary transitions between nonvariable and variable or polymorphic coloration have been accompanied by changes in the ecological variables we examined. Irrefutable demonstration of a role of color pattern variation in amphibian decline and in the dynamics and persistence of populations in general will require a manipulative experimental approach.     

Examining the relationship between local extinction risk and position in range

Over half of globally threatened animal species have experienced rapid geographic range loss. Identifying the parts of species’ distributions most vulnerable to local extinction would benefit conservation planning. However, previous studies give little consensus on whether ranges decline to the core or edge. We built on previous work by using empirical data to examine the position of recent local extinctions within species’ geographic ranges, address range position as a continuum, and explore the influence of environmental factors. We aggregated point‐locality data for 125 Galliform species from across the Palearctic and Indo‐Malaya into equal‐area half‐degree grid cells and used a multispecies dynamic Bayesian occupancy model to estimate rates of local extinctions. Our model provides a novel approach to identify loss of populations from within species ranges. We investigated the relationship between extinction rates and distance from range edge by examining whether patterns were consistent across biogeographic realm and different categories of land use. In the Palearctic, local extinctions occurred closer to the range edge than range core in both unconverted and human‐dominated landscapes. In Indo‐Malaya, no pattern was found for unconverted landscapes, but in human‐dominated landscapes extinctions tended to occur closer to the core than the edge. Our results suggest that local and regional factors override general spatial patterns of recent local extinction within species’ ranges and highlight the difficulty of predicting the parts of a species’ distribution most vulnerable to threat.     

Changes in Species Abundance, Distribution, and Diversity in a Central European Bird Community

We analyzed possible causes of changes in species abundance, range size, and diversity as well as extinctions and colonizations in a central European bird community. Using data from the semiquantitative "Lake Constance" breeding bird atlas, we demonstrated that changes in regional abundances from 1980–1981 to 1990–1992 of 151 coexisting bird species were influenced by breeding habitat and migratory status. Significant declines were found in populations of farmland species and long-distance migrants. Farmland species lost parts of their ranges but hardly changed in local abundance in sites where they still occurred. In contrast, declines in long-distance migrants were caused by significant declines in local abundance with only slight loss of occupied range. Regional extinctions and colonizations were predictable from overall population trends. For example, all species that went extinct were either farmland species or long-distance migrants. Avian community composition was influenced by disproportionate declines of abundant species. This led to declines in the total number of breeding pairs and in community biomass and to increases in community evenness, but to only slight declines in species richness. Future conservation efforts in Europe need to focus more on farmland species and on understanding causes for the declines of long-distance migrants.     

Hunting and the Likelihood of Extinction of Amazonian Mammals

Species inhabiting tropical forests are thought to be on the verge of mass extinction. Much work has focused on extinction rates caused by deforestation; however, many of the recorded extinctions that have occurred since 1600 were a result of overhunting. We collected data on the relative abundance of large-bodied mammals in the northeastern Peruvian Amazon in areas with persistent hunting pressure and in areas with infrequent hunting pressure. We quantified the effects of hunting by calculating the change in abundance of species between the infrequently and persistently hunted sites. We report that in Amazonian mammals weighing more than 1 kg the degree of population declines caused by hunting is correlated with the species' intrinsic rate of natural increase (r_max  ), longevity, and generation time. Our results show that species with long-lived individuals, low rates of increase, and long generation times are more vulnerable to extinction than species with short-lived individuals, high rates of increase, and shorter generations.     

Geometrical Factors and Metapopulation Dynamics of the Bush Cricket, Metrioptera bicolor Philippi (Orthoptera: Tettigoniidae)

This paper presents a metapopulation study of the bush cricket, Metrioptera bicolor , living in a recently fragmented landscape. The species inhabits grass and heathland patches of varying area and isolation. Analyses are made of how these geometrical factors affect local population size and density, distribution pattern, and the probability of local extinction and colonization. The proportion of available patches occupied varied between 72 and 79% during 1985–1990. Unoccupied patches were smaller and more isolated than those that were occupied. Patches where populations became extinct during this period were smaller than those with persisting populations. Since local population size was well correlated with patch area, it was clear that stochastic extinctions only occurred in small populations. Critical patch size for population extinction was approximately half a hectare. Colonized patches were less isolated than those that had not been colonized. Critical inter-patch distance for colonization was about 100 meters. The turnover was restricted to an identifiable share of the available patches. Only 33% of the patches were so small that extinction due to stochastic causes could be considered highly probable. This metapopulation will therefore most likely persist over a considerable period in its present spatial structure. There are apparent threats of further fragmentation, however, and nothing is known about the likelihood of large-scale extinctions resulting from extremely unfavorable weather conditions. Nevertheless, our results show that it is appropriate to include geometrical factors in metapopulation models.     

Extinction of Mammal Populations in Western North American National Parks

Patterns of local extinction of mammal populations in western North American parks were examined in relation to current biogeographic and population lifetime models. The analysis was based on species sighting records as of 1989. While western North American parks are obviously not true isolates, patterns of mammal extinction in them are nonetheless consistent with two predictions of the land-bridge island hypothesis. First, the number of extinctions has exceeded the number of colonizations since park establishment, and, second, the rate of extinction is inversely related to park area. Factors influencing the lifetime of mammal populations were evaluated using a stepwise multivariate survival analysis procedure for censored data. Survival time for mammal populations was positively related to estimated initial population size. After accounting for population size, species within the order Lagomorpha were particularly prone to extinction. Finally, after controlling for population size and taxon variation, survival time was positively related to age of maturity, indicating that species with longer generation times—age of maturity and generation time are highly correlated in mammals—persist longer in absolute time.     

Metapopulation Dynamics and Amphibian Conservation

Abstract: In many respects, amphibian spatial dynamics resemble classical metapopulation models, in which subpopulations in breeding ponds blink in and out of existence and extinction and colonization rates are functions of pond spatial arrangement. This "ponds-as-patches" view of amphibian spatial dynamics is useful in several respects. First, it highlights the importance of regional and landscape processes in determining local patterns of abundance. Second, it offers a straightforward, pond-based approach to monitoring and managing amphibian populations. For many species, however, the ponds-as-patches view may be an oversimplification and metapopulation structure may be more apparent than real. Changes in distribution may be caused by processes other than extinction and recolonization, and most extinctions probably result from deterministic factors, not stochastic processes. In addition, the effects of pond isolation appear to be important primarily in disturbed environments, and in many cases these isolation effects may be better explained by the distribution of terrestrial habitats than by the distribution of breeding ponds. These complications have important implications for both researchers and managers. For researchers, future efforts need to determine the mechanisms underlying patterns of abundance and distributional change and patterns in amphibian populations. For managers, effective conservation strategies must successfully balance metapopulation considerations with careful attention to local habitat quality. Furthermore, translocations and active management may be indispensable tools for conserving amphibians in landscapes containing multiple breeding ponds.     

Batrachochytrium dendrobatidis and the Collapse of Anuran Species Richness and Abundance in the Upper Manu National Park,Southeastern Peru

Abstract: Amphibians are declining worldwide, but these declines have been particularly dramatic in tropical mountains, where high endemism and vulnerability to an introduced fungal pathogen, Batrachochytrium dendrobatidis (Bd), is associated with amphibian extinctions. We surveyed frogs in the Peruvian Andes in montane forests along a steep elevational gradient (1200–3700 m). We used visual encounter surveys to sample stream‐dwelling and arboreal species and leaf‐litter plots to sample terrestrial‐breeding species. We compared species richness and abundance among the wet seasons of 1999, 2008, and 2009. Despite similar sampling effort among years, the number of species (46 in 1999) declined by 47% between 1999 and 2008 and by 38% between 1999 and 2009. When we combined the number of species we found in 2008 and 2009, the decline from 1999 was 36%. Declines of stream‐dwelling and arboreal species (a reduction in species richness of 55%) were much greater than declines of terrestrial‐breeding species (reduction of 20% in 2008 and 24% in 2009). Similarly, abundances of stream‐dwelling and arboreal frogs were lower in the combined 2008–2009 period than in 1999, whereas densities of frogs in leaf‐litter plots did not differ among survey years. These declines may be associated with the infection of frogs with Bd. B. dendrobatidis prevalence correlated significantly with the proportion of species that were absent from the 2008 and 2009 surveys along the elevational gradient. Our results suggest Bd may have arrived at the site between 1999 and 2007, which is consistent with the hypothesis that this pathogen is spreading in epidemic waves along the Andean cordilleras. Our results also indicate a rapid decline of frog species richness and abundance in our study area, a national park that contains many endemic amphibian species and is high in amphibian species richness.     

Long-Term Changes in the Avifauna of Barro Colorado Island, Panama, a Tropical Forest Isolate

Since its isolation from the mainland more than 85 years ago, 65 bird species have disappeared from Barro Colorado Island, Panama. Because of these extinctions the island is often used as a model for the study of faunal relaxation, or loss of species through time. The most recent survey of the island's bird community was completed in 1970. Between June 1994 and May 1996 I surveyed the island and observed 218 species, including 5 species never before recorded. Three relatively sedentary species have experienced severe population declines since Willis's 1970 survey and may be on the brink of disappearing from the island. Willis estimated 500 Slate-colored Grosbeaks ( Pitylus grossus ), whereas I found only two pairs of this conspicuous midstory-dwelling finch. Two cotingas—Speckled Mourner ( Laniocera rufescens ) and Rufous Piha ( Lipaugus unirufus )—have declined by 85–95%. I did not locate any individuals of 36 other species that were present during the 1970s. Most (21) of these are uncommon aquatic or nocturnal species, which I may have missed during my surveys, or are rare to uncommon edge species that probably move frequently to and from the island. Seven species, however, are primarily inhabitants of second-growth forest and have been lost probably because of continuing successional maturation of the forest, including changes in land use around the laboratory clearing. Seven forest-dwelling species disappeared during the 1970s and have not recolonized. I detected only one sedentary forest-dwelling species, Great Currasow ( Crax rubra ), that previously had been reported as missing from the island. The nearly complete lack of recolonizations by such forest-interior species suggests that local extinction from tropical forest isolates may be extremely persistent. Tropical forest reserves as small as Barro Colorado Island (1600 ha) may not preserve high levels of regional avian diversity over long periods of time.     

Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish.

A leading hypothesis of amphibian population declines is that combinations of multiple stressors contribute to declines. We examined the role that chemical contamination, competition, and predation play singly and in combination in aquatic amphibian communities. We exposed larvae of American toads (Bufo americanus), southern leopard frogs (Rana sphenocephala), and spotted salamanders (Ambystoma maculatum) to overwintered bullfrog tadpoles (R. catesbeiana), bluegill sunfish (Lepomis macrochirus), the insecticide carbaryl, and ammonium nitrate fertilizer in 1000-L mesocosms. Most significantly, our study demonstrated that the presence of multiple factors reduced survival of B. americanus and A. maculatum and lengthened larval periods of R. sphenocephala. The presence of bluegill had the largest impact on the community; it eliminated B. americanus and A. maculatum and reduced the abundance of R. sphenocephala. Chemical contaminants had the second strongest effect on the community with the insecticide, reducing A. maculatum abundance by 50% and increasing the mass of anurans (frogs and toads) at metamorphosis; the fertilizer positively influenced time and mass at metamorphosis for both anurans and A. maculatum. Presence of overwintered bullfrogs reduced mass and increased time to metamorphosis of anurans. While both bluegill and overwintered bullfrog tadpoles had negative effects on the amphibian community, they performed better in the presence of one another and in contaminated habitats. Our results indicate that predicting deleterious combinations from single-factor effects may not be straightforward. Our research supports the hypothesis that combinations of factors can negatively impact some amphibian species and could contribute to population declines.     

Extinction and Colonization of Birds on Habitat Islands

Abstract: We used point-count and transect surveys to estimate the distribution and abundance of eight scrub-breeding bird species in 34 habitat fragments and the urban matrix in southern California. We then calculated local extinction and colonization rates by comparing our data with surveys conducted in 1987. We classified factors that influence extinction and colonization rates into two types: (1) extrinsic factors, which are characteristics of the habitat fragments such as area, age, and isolation and (2) intrinsic factors, which are characteristics of the species that inhabit fragments, such as body size and population density. Over the past decade, at least one species went locally extinct in over 50% of the fragments, and local extinctions were almost twice as common as colonizations. Fragment size and, to a lesser extent, fragment age were the most important extrinsic factors determining extinction and colonization. Density indices of scrub birds were the most important intrinsic factors determining extinction rates, predicting the number of sites occupied, the probability of local extinction, relative area requirements, and time to local extinction.