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The global macroecology of brood size in amphibians reveals a predisposition of low‐fecundity species to extinction
Abstract
Aim
The diversity of brood size across animal species exceeds the diversity of most other life‐history traits. In some environments, reproductive success increases with brood size, whereas in others it increases with smaller broods. The dominant hypothesis explaining such diversity predicts that selection on brood size varies along climatic gradients, creating latitudinal fecundity patterns. Another hypothesis predicts that diversity in fecundity arises among species adapted to different microhabitats within assemblages. A more recent hypothesis concerned with the consequences of these evolutionary processes in the era of anthropogenic environmental change predicts that low‐fecundity species might fail to recover from demographic collapses caused by rapid environmental alterations, making them more susceptible to extinctions. These hypotheses have been addressed predominantly in endotherms and only rarely in other taxa. Here, we address all three hypotheses in amphibians globally.
Location
Global.
Time period
Present.
Major taxa studied
Class Amphibia.
Methods
Using a dataset spanning 2,045 species from all three amphibian orders, we adopt multiple phylogenetic approaches to investigate the association between brood size and climatic, ecological and phenotypic predictors, and according to species conservation status.
Results
Brood size increases with latitude. This tendency is much stronger in frogs, where temperature seasonality is the dominant driver, whereas salamander fecundity increases towards regions with more constant rainfall. These relationships vary across continents but confirm seasonality as the key driver of fecundity. Ecologically, nesting sites predict brood size in frogs, but not in salamanders. Finally, we show that extinction risk increases consistently with decreasing fecundity across amphibians, whereas body size is a “by‐product” correlate of extinction, given its relationship with fecundity.
Main conclusions
Climatic seasonality and microhabitats are primary drivers of fecundity evolution. Our finding that low fecundity increases extinction risk reinforces the need to refocus extinction hypotheses based on a suggested role for body size.
... Consequently, many of their models are based on small sample sizes, which could have led to inflated confidence intervals of slopes and thus numbers of traits resulting to be independent of body mass. In fact, there are other studies that found a scaling to body mass for traits that Hallmann and Griebeler (2020) reported as independent of body mass (Kaplan and Salthe 1979;Pincheira-Donoso et al. 2021;Salthe 1969). Moreover, several allometric models on amphibian clutch size and egg size are presented in other studies (Furness, Venditti, and Capellini 2022;Gomez-Mestre, Pyron, and Wiens 2012;Kupfer et al. 2016;Monroe, South, and Alonzo 2015;Pincheira-Donoso et al. 2021;Prado and Haddad 2005;Salthe 1969;Wells 2007), but conversely to Hallmann and Griebeler (2020), the majority used species' snoutvent length (SVL) instead of body mass, because information on SVL is more frequent in the literature (Santini et al. 2018). ...
... In fact, there are other studies that found a scaling to body mass for traits that Hallmann and Griebeler (2020) reported as independent of body mass (Kaplan and Salthe 1979;Pincheira-Donoso et al. 2021;Salthe 1969). Moreover, several allometric models on amphibian clutch size and egg size are presented in other studies (Furness, Venditti, and Capellini 2022;Gomez-Mestre, Pyron, and Wiens 2012;Kupfer et al. 2016;Monroe, South, and Alonzo 2015;Pincheira-Donoso et al. 2021;Prado and Haddad 2005;Salthe 1969;Wells 2007), but conversely to Hallmann and Griebeler (2020), the majority used species' snoutvent length (SVL) instead of body mass, because information on SVL is more frequent in the literature (Santini et al. 2018). Yet, the use of SVL hampers any comparison of allometric models within amphibians and to other vertebrate groups due to differences in animal body shapes. ...
... The six traits related to fecundity (egg diameter, egg volume, clutch size, clutch volume, annual clutch number and annual clutch volume) were all positively correlated to adult body mass, except for clutch volume in caecilians, and for both annual clutch number and annual clutch volume in salamanders and in all amphibians together. Thus, we confirm previous studies reporting that egg diameter and clutch size increase with body size in all three orders (Gomez-Mestre, Pyron, and Wiens 2012; Hallmann and Griebeler 2020;Kupfer et al. 2016;Pincheira-Donoso et al. 2021;Salthe 1969;Wells 2007), but we challenge previous studies finding no relation of body size to egg mass (proportional to egg volume) and egg diameter in frogs, and to clutch size in salamanders (Hallmann and Griebeler 2020;Hartmann, Hartmann, and Haddad 2010;Silva et al. 2020). ...
Amphibians have the least studied life histories among vertebrates, although they have unique and the most diverse life histories within this group. We compiled a new dataset on adult body mass and 16 other life history traits of 2069 amphibian species across three orders (1796 frogs, 236 salamanders, 37 caecilians). These traits characterise fecundity, offspring development from egg deposition to metamorphosis and adult life. We established allometric models on traits for all amphibians and each of the three orders to assess a potential scaling of traits to body mass and then checked whether allometric slopes were consistent with two different metabolic scaling exponents. Further, we examined a possible fast‐slow continuum in all amphibians, as well as in each of the two orders frogs and salamanders by applying principal component analysis (PCA) to five traits. Our allometric models indicated a positive scaling to body mass for 11 traits across all amphibians, 12 in frogs, and 10 in salamanders, and for five out of eight traits analysed in caecilians. Allometric slopes on most traits characterising offspring development were not significant. All slopes did not support a three‐quarter metabolic scaling exponent, whereas slopes on age at maturity and maximum longevity were consistent with an amphibian metabolic scaling exponent of 0.88. As in fishes, reptiles, birds, and mammals, the first axes of our PCAs indicated a body mass‐dependent fast‐slow continuum in amphibians. Amphibian species of slow life histories have larger body masses, later sexual maturities and longer lifespans and lay more and larger eggs than species of fast life histories, a pattern also known from reptiles. The second axes indicated a trade‐off between egg size and number. As this trade‐off was nearly independent of body mass, we hypothesise that amphibians have occupied a broad range of ecological niches without evolutionary changes in body mass.
... Extinctions are the outcome of progressive processes of population declines until a 'tipping point' where the degree of demographic collapse that prevents a species from recovering is reached (Cardillo et al., 2005;Sinervo et al., 2010;Collen et al., 2011;Hoffmann & Sgr o, 2011;Chaparro-Pedraza, 2021;Pincheira-Donoso et al., 2021). The circumstances that trigger the onset of these processes of decline can be multiple, but they have in common an alteration in the interactions between environmental conditions and the traits that species have evolved to face those conditions (Ferriere, Dieckmann & Couvet, 2004;Hoglund, 2009;Hoffmann & Sgr o, 2011;Pincheira-Donoso et al., 2021), i.e. when patterns of natural selection change at rates that exceed a species' ability to respond or adapt to such changes (Parmesan, 2006;Brook, Sodhi & Bradshaw, 2008;Dirzo et al., 2014;Murray et al., 2014;Chaparro-Pedraza, 2021). ...
... Extinctions are the outcome of progressive processes of population declines until a 'tipping point' where the degree of demographic collapse that prevents a species from recovering is reached (Cardillo et al., 2005;Sinervo et al., 2010;Collen et al., 2011;Hoffmann & Sgr o, 2011;Chaparro-Pedraza, 2021;Pincheira-Donoso et al., 2021). The circumstances that trigger the onset of these processes of decline can be multiple, but they have in common an alteration in the interactions between environmental conditions and the traits that species have evolved to face those conditions (Ferriere, Dieckmann & Couvet, 2004;Hoglund, 2009;Hoffmann & Sgr o, 2011;Pincheira-Donoso et al., 2021), i.e. when patterns of natural selection change at rates that exceed a species' ability to respond or adapt to such changes (Parmesan, 2006;Brook, Sodhi & Bradshaw, 2008;Dirzo et al., 2014;Murray et al., 2014;Chaparro-Pedraza, 2021). Extinctions are, therefore, a demographically progressive process that can be anticipated based on the signatures that population trends leave in species through time (Collen et al., 2011;Chaparro-Pedraza, 2021), in contrast with conservation categories. ...
... For example, one speciesbased approach has focussed on 'extinction models' which aim to identify characteristics in common among threatened species, ultimately defining the 'type' of species likely to be at risk (Purvis et al., 2000;Fisher & Owens, 2004;Cardillo et al., 2008;Kuussaari et al., 2009). Small geographic range size, low fecundity and body size (the direction of effect differing by taxonomic group and size-selective environmental threats) are frequently used predictors of extinction risk across taxa (Pimm, Jones & Diamond, 1988;Cardillo et al., 2005;Dirzo et al., 2014;Murray et al., 2014;Verde Arregoitia, 2016;Ripple et al., 2017;Ruland & Jeschke, 2017;Pincheira-Donoso et al., 2021). However, given that the majority of these studies utilise conservation categories as proxies of extinction risk, we still need to learn more about the traits associated with population declines (but see Collen et al., 2011;Murray et al., 2011) traits that could be indicators of future extinction risk, given that populations decline before a species becomes threatened. ...
The global-scale decline of animal biodiversity ('defaunation') represents one of the most alarming consequences of human impacts on the planet. The quantification of this extinction crisis has traditionally relied on the use of IUCN Red List conservation categories assigned to each assessed species. This approach reveals that a quarter of the world's animal species are currently threatened with extinction, and 1% have been declared extinct. However, extinctions are preceded by progressive population declines through time that leave demographic 'footprints' that can alert us about the trajectories of species towards extinction. Therefore, an exclusive focus on IUCN conservation categories, without consideration of dynamic population trends, may underestimate the true extent of the processes of ongoing extinctions across nature. In fact, emerging evidence (e.g. the Living Planet Report), reveals a widespread tendency for sustained demographic declines (an average 69% decline in population abundances) of species globally. Yet, animal species are not only declining. Many species worldwide exhibit stable populations, while others are even thriving. Here, using population trend data for >71,000 animal species spanning all five groups of vertebrates (mammals, birds, reptiles, amphibians and fishes) and insects, we provide a comprehensive global-scale assessment of the diversity of population trends across species undergoing not only declines, but also population stability and increases. We show a widespread global erosion of species, with 48% undergoing declines, while 49% and 3% of species currently remain stable or are increasing, respectively. Geographically, we reveal an intriguing pattern similar to that of threatened species, whereby declines tend to concentrate around tropical regions, whereas stability and increases show a tendency to expand towards temperate climates. Importantly, we find that for species currently classed by the IUCN Red List as 'non-threatened', 33% are declining. Critically, in contrast with previous mass extinction events, our assessment shows that the Anthropocene extinction crisis is undergoing a rapid biodiversity imbalance, with levels of declines (a symptom of extinction) greatly exceeding levels of increases (a symptom of ecological expansion and potentially of evolution) for all groups. Our study contributes a further signal indicating that global biodiversity is entering a mass extinction, with ecosystem heterogeneity and functioning, biodiversity persistence, and human well-being under increasing threat.
... The relative time spent in aquatic and terrestrial life-stages determines the identity and severity of threats posed to amphibian taxa. In addition, the traits that characterize different amphibian life-history strategies are predicted to influence species' susceptibility to anthropogenic threats, such that species with "faster" life histories are more likely to recover from declines (Pimm et al., 1988;Bennett and Owens, 1997;Hutchings et al., 2012;Pincheira-Donoso et al., 2021). Accordingly, threat status on the IUCN Red List has been related to mode of fertilization (internal vs external), clutch size, egg deposition site, and degree of parental care in several taxa (Hero et al., 2005;Bielby et al., 2008;Sodhi et al., 2008;González-del-Pliego et al., 2019;Pincheira-Donoso et al., 2021). ...
... In addition, the traits that characterize different amphibian life-history strategies are predicted to influence species' susceptibility to anthropogenic threats, such that species with "faster" life histories are more likely to recover from declines (Pimm et al., 1988;Bennett and Owens, 1997;Hutchings et al., 2012;Pincheira-Donoso et al., 2021). Accordingly, threat status on the IUCN Red List has been related to mode of fertilization (internal vs external), clutch size, egg deposition site, and degree of parental care in several taxa (Hero et al., 2005;Bielby et al., 2008;Sodhi et al., 2008;González-del-Pliego et al., 2019;Pincheira-Donoso et al., 2021). ...
... The safe harbor provided by mothers of these species may, unfortunately, generate a life history that is intrinsically more sensitive to anthropogenic stressors. The intrinsic connections between developmental mode, clutch size, species range size, and biogeography often put terrestrial species at greater risk (Lion et al., 2019;Pincheira-Donoso et al., 2021). The inherently unpredictable nature of aquatic environments and instability of complex life cycles (Istock, 1967) produces more of a bet-hedging strategy in classic amphibians that may serve them well in light of anthropogenic change. ...
Understanding how natural selection determines species’ life histories can reveal their resilience or sensitivity to anthropogenic changes. For example, the safe harbor hypothesis posits that natural selection will favor life histories that maximize the time spent in the safest life stages; a second theoretical prediction suggests that species with complex life histories will maximize the growth potential of a life stage relative to its safety. Amphibians exhibit complex life histories, with a diversity of developmental strategies occurring across taxa. Many strategies involve the complete elimination of a particular life stage, and thus provide an excellent opportunity to evaluate the main tenets of the safe harbor hypothesis and understand the consequences of this developmental variation for conservation of threatened amphibians. We develop a general framework for understanding developmental life histories of amphibians – including the special cases of paedomorphism, direct development, and viviparity – based on the relative growth potential and safety offered by aquatic and terrestrial habitat, which we tested using a global trait database. We then compare the IUCN Red List status of species differing in developmental mode, revealing that most fully aquatic species and species with an aquatic larval stage are currently of Least Concern, despite the fact that freshwater habitats are being lost at a much faster rate compared with terrestrial ecosystems. The higher proportion of direct developing and viviparous species that are threatened can be attributed to their smaller ranges, the fact that they are more likely to be found in rainforest habitats, and their relatively slow life histories. We conclude that an amphibian’s developmental mode reflects the relative costs and benefits of different habitats, and that this could contribute to the resilience or vulnerability of amphibians to future anthropogenic change.
... Surprisingly, despite much research, it is still unclear whether and how selective pressures related to environmental conditions and type of parental care drive evolutionary changes in the offspring size-number trade-off [9][10][11][12][13][14][15][16][17][18][19][20]. Answering this question is fundamental not only for advancing theory, but also because these life history traits influence the demographic trajectory of natural and introduced populations [21][22][23][24][25] and their ability to overcome many anthropogenic stressors [24,[26][27][28]. For example, in several taxa, fecundity influences extinction risk [27,29], population growth rate [30], invasion success [21,22], and the ability to thrive in urban, or more generally human-modified, habitats [26,28]. ...
... Answering this question is fundamental not only for advancing theory, but also because these life history traits influence the demographic trajectory of natural and introduced populations [21][22][23][24][25] and their ability to overcome many anthropogenic stressors [24,[26][27][28]. For example, in several taxa, fecundity influences extinction risk [27,29], population growth rate [30], invasion success [21,22], and the ability to thrive in urban, or more generally human-modified, habitats [26,28]. Here, we test hypotheses predicting that parental care or terrestrial habitats in which offspring develop alter the offspring size-number trade-off, specifically leading to smaller clutches of larger eggs, in a sample of over 800 amphibian species. ...
... Offspring number rather than offspring size may, however, be the target of selection. EnvironmentalAU : PleasecheckandconfirmthattheeditstothesentenceEnvironmentalconditionscandrive conditions can drive brood size evolution [19,27] since they determine the uploaded as S1 Data. The sources for the data are available in S1 Data and list in S3 Data. ...
The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.
... Life-history variation underlies the whole spectrum of demographic processes (Stearns 1976), from the pace of adaptive change to the risk of population declines that lead to extinction (Gaillard et al. 2005, Ripple et al. 2017, Pincheira-Donoso et al. 2021. The aggregated influence of life history traits on such demographic processes is often reflected in species generation lengths -the average age of parents of the current cohort (i.e. ...
... Finally, our estimates can also inform macroecological and evolutionary studies. As life histories generally follow altitudinal or latitudinal gradients (Morrison and Hero 2003, Cvetković et al. 2009, Alice Boyle et al. 2016, Meiri et al. 2020, Pincheira-Donoso et al. 2021, our estimates can potentially inform studies linking life histories and geographical patterns at global scales (e.g. generation time changes across latitudinal gradients), as well as inform studies on the potential influence of life histories on the evolutionary processes at global scales (e.g. life histories and genome size; Liedtke et al. 2018). ...
Variation in life histories influences demographic processes, from adaptive changes to population declines leading to extinction. Among life history traits, generation length offers a critical feature to forecast species' demographic trajectories such as population declines (widely used by the IUCN Red List) and adaptability to environmental change over time. Therefore, estimates of generation length are crucial to monitor demographic stability or predict future changes in highly threatened organisms, particularly amphibians and reptiles, which are particularly threatened among vertebrates and for which uncertainty in future impacts remains high. Despite its importance, generation length for amphibians and reptiles is largely missing. Here, we aim to fill in this gap by modeling generation lengths for amphibians, squamates and testudines as a function of species size, climate, life history and phylogeny using generalized additive models and phylogenetic generalized least squares. We estimated generation lengths for 5059 (57%) amphibians, 8722 (73%) squamates and 117 (32%) testudines. Our models performed well for most families (e.g. Bufonidae among amphibians, Lacertidae and Colubridae among squamates, and Geoemydidae among testudines) while we found high uncertainty around the prediction of a few families, notably Chamaeleonidae. Species' body size and mean temperature were the main predictors of generation length in all groups. Although our estimates are not meant to substitute robust and validated measurements from field studies or natural history museums, they can help reduce existing biases in conservation assessments until field data is comprehensively available.
... Life history variation underlies the whole spectrum of demographic processes, from the pace of adaptive change to the risk of population declines that lead to extinction (Pincheira-Donoso et al., 2021;Ripple et al., 2017). The aggregated influence of life history traits on such demographic processes is often represented by species generation lengthsthe average age of parents of the current cohort (i.e., newborn individuals in the population; Charlesworth, 1994;Gingerich, 2019;IUCN Standards and Petitions Committee, 2022). ...
... Our estimates can play a crucial role in climate change adaptability studies.Finally, our estimates can also inform macroecological and evolutionary studies. As life histories generally follow altitudinal or latitudinal gradient Meiri et al., 2020;Morrison & Hero, 2003;Pincheira-Donoso et al., 2021), our estimates can potentially inform studies linking life histories and the geographical patterns, as well as inform studies on the potential influence of life histories on the evolutionary process at global scale(Liedtke et al., 2018). ...
Variation in life histories influences demographic processes from adaptive changes to population declines leading to extinction. Among life history traits, generation length offers a critical feature to forecast species’ demographic trajectories such as population declines (widely used by the IUCN Red List of Threatened Species) and adaptability to environmental change over time. Therefore, estimates of generation length are crucial to monitor demographic stability or future change in highly threatened organisms, particularly ectothermic tetrapods (amphibians and reptiles) – which rank among the most threatened groups – but for which uncertainty in future impacts remains high. Despite its importance, generation length for amphibians and reptiles is largely missing. Here, we aimed to fill-in this gap by modeling generation lengths for amphibians, squamates and testudines as a function of species size, climate, life history, and phylogeny using generalized additive models and phylogenetic generalized least squares. We obtained estimates of generation lengths for 4,543 (52%) amphibians, 8,464 (72%) squamates and 118 (32%) testudines. Our models performed well for most families, for example Bufonidae in amphibians, Lacertidae and Colubridae in squamates and Geoemydidae in testudines, while we found high uncertainty around the prediction of a few families, notably Chamaeleonidae. Species’ body size and mean temperature were the main predictors of generation length in all groups. Although our estimates are not meant to substitute robust and validated measurements from field studies or natural history museums, they can help reduce existing biases in conservation assessments until field data will be comprehensively available.
... We expect that both bird and mammal pollinators would show different hotspots of species richness patterns across the geographical regions of India due to differences in their ability to move between habitats. We also predict that the risk of extinction and population declines of bird and mammal pollinators will increase with body size given the increased probability of hunting in association with the tendency of large-sized endotherms for low reproductive rates, which impacts on their chances of rapid demographic recovery (Purvis et al. 2000;Cardillo et al. 2005;Hutchings et al. 2012;Comeros-Raynal et al. 2016;Verde Arregoitia 2016;Ripple et al. 2017, Pincheira-Donoso et al. 2021. Similarly, we predict that species with small geographic range sizes and low-density populations are more predisposed to extinction risk since they are more vulnerable to local catastrophes and demographic stochasticity, as well as inbreeding events (Kattan 1992;Manne et al. 1999;Gaston and Fuller 2009;Pincheira-Donoso and Hodgson 2018;Chichorro et al. 2019;Shuai et al. 2021). ...
... To investigate threats to bird and mammal pollinators we categorized species into threatened or non-threatened as per the IUCN categories, where Vulnerable (VU), Endangered (EN) and Critically Endangered (CR) species were considered as threatened, and the remaining categories (Least Concern (LC) and Near Threatened (NT)) non-threatened. We then employed the IUCN 'consensus approach' explained below to calculate the proportion of threatened species (PropThreat) (Clausnitzer et al. 2009;Hoffmann et al. 2010;Böhm et al. 2013, Pincheira-Donoso et al. 2021. As per the formula: PropThreat = (CR + EN + VU)/(N -DD), where N is the total number of species in the sample per category and DD is the number of species in the Data Deficient category. ...
Animal pollinators underpin the functioning and persistence of ecosystems globally. However, the vital role of pollination is being progressively eroded by the worldwide decline of pollinator species caused by human-induced environmental degradation, resulting in rising costs to biodiversity, agriculture, and economy. Most studies quantifying pollinator diversity and declines have focused on insects, whereas vertebrate pollinators remain comparatively neglected. Here, we present the first comprehensive study quantifying the macroecological patterns of species richness and extinction risk of bird and mammal pollinators in India, a region of extremely high biodiversity and increasing anthropogenic pressure. Our results reveal that hotspots of mammal pollinator diversity are restricted to the south of the Western Ghats, whereas bird pollinator diversity hotspots are scattered throughout the country. Analyses of hotspots of threatened species (based on the IUCN Red List) show that only mammal pollinators are currently classified as threatened in India, whereas multiple hotspots of population declines were observed for birds, and primarily in the Southwest for mammal pollinators. Our analyses failed to identify a role for species traits as drivers of these patterns, whereas most pollinators appear to be threatened by agriculture, logging and hunting for food, and medicinal purposes. Pollinator endangerment has widescale ecological and economic implications such as reduced food production, plant extinction, loss of functional and genetic diversity, and economic damage. We suggest protection of vertebrate pollinators should be emphasised in active conservation agendas in India.
... However, the color pattern between the male and females was distinct, with the females having a broader dark grey dorsal color and a narrower yellow lateral stripe than males, and the males a dark grey color with mottled spots on the back (Fig. 3). The known clutch sizes among caecilians ranges from 3-144 (Pincheira-Donoso et al. 2021). The clutch size of I. kodaguensis was 14 eggs (Fig. 6), which is a much lower clutch size than the other Western Ghats species, I. beddomei (n = ~30 eggs) and I. bombayensis (n = ~60 eggs) (Seshachar et al. 1982;Bhatta 1999;Jadhav et al. 2007). ...
... The clutch size of I. kodaguensis was 14 eggs (Fig. 6), which is a much lower clutch size than the other Western Ghats species, I. beddomei (n = ~30 eggs) and I. bombayensis (n = ~60 eggs) (Seshachar et al. 1982;Bhatta 1999;Jadhav et al. 2007). According to Pincheira-Donoso et al. (2021), amphibians with lower fecundity are more predisposed to extinction risk than those with larger clutch sizes. ...
Of the amphibian orders, the Gymnophiona (caecilians) have the smallest number of species and are the least known. We report new information on the morphology, biology, range, and distribution of Ichthyophis kodaguensis, a striped ichthyophiid caecilian from the Western Ghats, India, that shows the first evidence of possible sexual dimorphism in this species. Based on the clutch size, limited range, relatively low fecundity, and agricultural practices in their habitats, we consider that I. kodaguensis is highly threatened when compared to other striped ichthyophiids from the Western Ghats biodiversity hotspot.
... Amphibians are characterized by traits that make them more prone to be negatively affected by global changes than other vertebrates, such as small geographic ranges, limited dispersal ability, dependence on water bodies, and limited thermoregulating abilities and sensitivity to evaporation (Duellman and Trueb 1994;Ficetola et al. 2015). However, while previous studies have shown that biological traits such as body size, geographic range size, or brood size play a key role in predicting amphibian RL extinction risk (Cardillo 2021;Cooper et al. 2008;Fontana et al. 2021;Pincheira-Donoso et al. 2021a;Sodhi et al. 2008), the effects of climate change remain poorly known. ...
... For each species, we compiled information from existing datasets (IUCN 2021;Oliveira et al. 2017;Pincheira-Donoso et al. 2021a;Pincheira-Donoso et al. 2021b) for 32 biological traits such as nesting site, microhabitat, parity mode, diet, daily/seasonal activity pattern, number of habitats, and body size (Table A1). To account for species phylogeny, we extracted the first six eigenvectors from the phylogeny in Jetz et al. 2018, which explained 96% of the total variance (Table A3). ...
Assessing the extinction risk of species through the IUCN Red List is key to guiding conservation policies and reducing biodiversity loss. This process is resource-demanding, however, and requires a continuous update which becomes increasingly difficult as new species are added to the IUCN Red List. The use of automatic methods, such as comparative analyses to predict species extinction risk, can be an efficient alternative to maintaining up to date assessments. Using amphibians as a study group, we predict which species were more likely to change status, in order to suggest species that should be prioritized for reassessment. We used species traits, environmental variables, and proxies of climate and land-use change as predictors of the IUCN Red List category of species. We produced an ensemble prediction of IUCN Red List categories by combining four different model algorithms: Cumulative Link Models (CLM), phylogenetic Generalized Least Squares (PGLS), Random Forests (RF), Neural Networks (NN). By comparing IUCN Red List categories with the ensemble prediction, and accounting for uncertainty among model algorithms, we identified species that should be prioritized for future reassessments due to high prediction versus observation mismatch. We found that CLM and RF performed better than PGLS and NN, but there was not a clear best algorithm. The most important predicting variables across models were species range size, climate change, and land-use change. We propose ensemble modelling of extinction risk as a promising tool for prioritizing species for reassessment while accounting for inherent models' uncertainty.
... It should be noted that, while we used body mass as a proxy for species' susceptibility, other traits may be more suitable for different taxa. For instance, traits such as the number of reproductive events per year may be more relevant for amphibians, as they better reflect the capacity of amphibian populations to reproduce and withstand increased road mortality and other adverse impacts (Pincheira-Donoso et al., 2021). ...
Roads, while crucial for human development and economic growth, pose significant threats to biodiversity. Large-scale road risk assessments are essential for guiding infrastructure planning, particularly in identifying areas to avoid new construction or prioritizing regions for mitigation where road networks are already established. However, conducting comprehensive assessments is challenging in regions with limited data on species' responses to roads. In this study, we propose a methodological approach for global and regional risk assessments of road-related impacts, utilizing data on road exposure and species-level susceptibility to road effects. We first derive species-specific susceptibility to road impacts using available trait data and expert knowledge. This information is spatialized through species range maps, creating a cross-taxa susceptibility layer. We then combine this layer with infrastructure density data to produce a bivariate map that highlights the co-occurrence of susceptibility and exposure. Through this approach, we identify priority mitigation areas-regions with high susceptibility and high exposure where mitigation efforts should be concentrated-and priority preservation areas-regions with high susceptibility but low exposure that should be protected from further road development. Our case-study focuses on mustelids, a globally distributed group with significant vulnerability to road impacts yet un-derrepresented in road ecology studies. The results reveal that the highest-risk areas are concentrated in Eastern Europe, Southeast Asia, and scattered across sub-Saharan Africa, where high conservation value intersects with extensive road networks, marking these as priority mitigation areas. Priority preservation areas span mainly across South America, North America, and Siberia, with some areas across Africa and Borneo. This framework offers a foundation for preliminary assessments and proactive zoning, aiding in the identification of conservation management areas across different infrastructure types and taxa. Its adaptability makes it a valuable tool for researchers, wildlife managers, and transportation planners conducting large-scale assessments of infrastructure impacts on biodiversity.
... Most conservation initiatives for amphibians today focus on ex-situ breeding programs in different facilities (e.g., zoos, aquariums and botanical gardens), with the ultimate goal of releasing suitable candidates into natural or restored habitats (Griffiths and Pavajeau, 2008;Harding et al., 2016;Bradfield et al., 2023). From a life-history point of view, amphibians are highly suitable for ex-situ conservation measures, due to several characteristics: their body size is comparatively small and requires very little space, they possess high fecundity, short generation time, and lack parental care (Smith and Sutherland, 2014;Tapley et al., 2015;Pincheira-Donoso et al., 2021). They also have relatively small home ranges compared to mammals and birds (Trochet et al., 2014), and in some cases, they cope with captivity, both physiologically and behaviourally, better than some other taxa (Biega et al., 2017). ...
The increasing rate of biodiversity loss and the number of threatened or endangered species worldwide has
accelerated conservation and recovery strategies, emphasising fish, birds, and mammals. This focus has mostly
neglected amphibians, which are currently facing the most existential crisis among all vertebrates, with declining
populations across most habitats. The factors driving global amphibian declines are diverse, often synergistic,
and predominantly anthropogenic. Amphibians urgently require rapid conservation action, and we cannot afford
to wait while the most important critical elements required to initiate effective recovery efforts are known. We
recommend the rapid (re)introduction of this “forgotten” taxon via the guidelines of trophic rewilding.
Amphibian rewilding initiatives may provide early indications of ecological health and better contribute to
conservation goals, by simultaneously protecting highly endangered species, and promoting ecological stability
in these species ecosystems
... Moreover, we found that climate instability is a better predictor than contemporary climate to amphibians and both climates has similar strength to mammals, while the contemporary climate is the unique predictor to birds and squamates. Importantly, as current macroecological theory frequently uses patterns observed in endotherms to generalize to ectotherms (see Pincheira-Donoso et al., 2021), our findings demonstrate that endotherms and ectotherms have distinct macroecological patterns and provide an enhanced mechanism for explain the macroecology of ectotherms. ...
Although climate‐based hypotheses are widely used to explain large‐scale diversity patterns, they fall short of explaining the spatial variation among taxonomic groups. Integrating food web and metabolic theories into macroecology is a promising step forward, as they allow including explicit taxon‐specific traits that can potentially mediate the relationship between climate and diversity. Our investigation focuses on the role of body size and trophic structure in mediating the influence of contemporary climate and historical climate change on global tetrapods species richness. We used piecewise structural equation modeling to assess the direct effects of contemporary climate and climate instability of species richness and the indirect effects of climate on tetrapod richness mediated by community‐wide species traits. We found that birds and mammals are less sensitive to the direct effect of contemporary climate than amphibians and squamates. Contemporary climate and climate instability favored the species richness of mammals and amphibians. However, for birds and squamates, this link is only associated with contemporary climate. Moreover, we showed that community‐wide traits are correlated with species richness gradients. However, we highlight that this relationship is dependent upon the specific traits and taxonomic groups. Specifically, bird communities with smaller bodies and bottom‐heavy structures support higher species richness. Squamates also tend to be more diverse in communities with prevalence of smaller bodies, while mammals are correlated with top‐heavy structures. Moreover, we showed that higher contemporary climate and climate instability reduce the species richness of birds and mammals through community‐wide traits and indirectly increase squamate species richness. We also showed that body size and trophic structure are driving a global asymmetric response of tetrapod diversity to climate effects, which highlights the limitation to use the “typical” climate‐based hypotheses. Furthermore, by combining multiple theories, our research contributes to a more realistic and mechanistic understanding of diversity patterns across taxonomic groups.
... More specifically, we propose the hypothesis that rapid economic (and ecological) impacts will be more likely in species with a trait profile that combines potential for both exaptation (i.e., previously acquired traits that make them demographically viable upon introduction, enabling rapid establishment) and adaptation (i.e., the demographic resilience from traits that facilitated exaptation enhance likelihood for adaptation to remaining environmental demands that could still impact on overall fitness) to the newly introduced environments. The rapid emergence of comprehensive global-scale databases on entire lineages (e.g., Jones et al., 2009;Meiri, 2018;Pincheira-Donoso et al., 2021;Tobias et al., 2022), coupled with machine learning technology for analyses of complex interactions and for accurate predictions, offer unprecedented opportunities to identify species profiles with high potential for rapid economic impacts. ...
A dominant syndrome of the Anthropocene is the rapid worldwide spread of invasive species with devastating environmental and socio-economic impacts. However, the dynamics underlying the impacts of biological invasions remain contested. A hypothesis posits that the richness of impactful invasive species increases proportionally with the richness of non-native species more generally. A competing hypothesis suggests that certain species features disproportionately enhance the chances of non-native species becoming impactful, causing invasive species to arise disproportionately relative to the numbers of non-native species. We test whether invasive species with reported monetary costs reflect global numbers of established non-native species among phyla, classes, and families. Our results reveal that numbers of invasive species with economic costs largely reflect non-native species richness among taxa (i.e., in 96 % of families). However, a few costly taxa were over- and under-represented, and their composition differed among environments and regions. Chordates, nematodes, and pathogenic groups tended to be the most over-represented phyla with reported monetary costs, with mammals, insects, fungi, roundworms, and medically-important microorganisms being over-represented classes. Numbers of costly invasive species increased significantly with non-native richness per taxon, while monetary cost magnitudes at the family level were also significantly related to costly invasive species richness. Costs were biased towards a few ‘hyper-costly’ taxa (such as termites, mosquitoes, cats, weevils, rodents, ants, and asters). Ordination analysis revealed significant dissimilarity between non-native and costly invasive taxon assemblages. These results highlight taxonomic groups which harbour disproportionately high numbers of costly invasive species and monetary cost magnitudes. Collectively, our findings support prevention of arrival and containment of spread of non-native species as a whole through effective strategies for mitigation of the rapidly amplifying impacts of invasive species. Yet, the hyper- costly taxa identified here should receive greater focus from managers to reduce impacts of current invasive species.
... Direct developers have particular life history and ecological traits, such as an association with high-altitude environments, restricted distributions, and smaller clutches with larger eggs, traits that can be associated with extinction risk [5,71,[98][99][100][101]. As verified here, the occurrence of direct developing species of Atlantic Forest anuran communities was mostly associated with temperature seasonality and potential evapotranspiration, hence, future climatic changes can impoverish these communities, especially by the loss of this group of species. ...
Different environmental and biological factors can originate and support different alternative life histories in different taxonomic groups. Likewise, these factors are important for the processes that assemble and structure communities. Amphibians, besides being highly susceptible to environmental conditions, have various reproductive strategies, such as the direct development of individuals. Several hypotheses have been raised about possible selective pressures related to the emergence of direct development in anurans, as well as the relationship between environmental characteristics and the occurrence of these species. Such investigations, however, have mainly focused on specific clades and/or regions. Here, we use structural equation modelling to investigate the relationships between different abiotic (temperature, precipitation, humidity, and terrain slope) and biotic (phylogenetic composition and functional diversity) factors and the proportion of species with direct development in 766 anuran communities of the Atlantic Forest, a biome with a vast diversity of anuran species and high environmental complexity. Anuran communities with higher proportions of direct developing species were found to be mainly influenced by low potential evapotranspiration, low temperature seasonality, and high functional diversity. Phylogenetic composition and terrain slope were also found to be important in determining the occurrence of these species in Atlantic Forest communities. These results show the importance of these factors in the structuring of these communities and provide important contributions to the knowledge of direct development in anurans.
... Reproduction is an energetically expensive component of a female's life history Healy et al., 2019), and for egg-laying species, there is substantial variation in within and between-species reproductive output parameters such as clutch size, number of clutches, and clutch intervals (Roff, 2002;Dochtermann and Gienger, 2012;Pincheira-Donoso and Hunt, 2017;Barneche et al., 2018;Meiri et al., 2020;Fisher et al., 2021;Pincheira-Donoso et al., 2021). Maternal investments in reproduction, which might be plastic or evolutionary in response to changes in local environmental conditions across clines, may influence inter-and intraspecific reproductive output diversity among egg-laying species (Ramakers et al., 2018;Meiri et al., 2020). ...
Global patterns in clutch size variations across species have been linked to resource availability and seasonal climate change. However, our understanding of the specific local-scale drivers of clutch size diversity has remained unclear, especially among populations of ectotherms with relatively homogeneous genetic structures experiencing varying local environmental conditions. And understanding the specific local-scale drivers of clutch size diversity within species can provide insight into the local adaptation of species or the evolution of key life history traits. Here, we collected clutch size data of a wide-ranging female lizard (Eremias argus) from field observation and literature across populations of varying elevations and latitudes in China. We then used mixed-effects models to test the relationship between clutch size, body size, habitat type, elevation, latitudes, and climate conditions. Unsurprisingly, body size was positively correlated with clutch size variations across all populations. When we accounted for body size, females from populations at higher latitudes had larger clutches, while females in less variable rainfall environments had smaller clutches. Interestingly, we found that females occupying higher geographic gradients (e.g., latitude and elevation) with certain habitats (e.g., grasslands and farmlands) were associated with larger clutch sizes. Thus, our study shows support for similar global macro-ecological drivers of clutch size diversity among lizard species, and also suggests that female ectotherms might have different reproductive decisions employed in response to local climates to maximise population replacement.
... Within both lineages, alarming proportions of species are known to be undergoing progressive population declines 2 , and 41% of amphibians and 21% of reptiles are listed as facing extinction risk under IUCN red list categories 38 . In addition to land-use change 40,41 , disease outbreaks 42,43 , and alien species invasions 44,45 , climate change has been implicated as one of the major factors involved in the decline of amphibian and reptile abundance both directly 46,47 and indirectly (e.g., by increasing susceptibility to disease 48 , or enhancing demographic susceptibility to declines 49 ). ...
Protected Areas (PAs) are the cornerstone of biodiversity conservation. Here, we collated distributional data for >14,000 (~70% of) species of amphibians and reptiles (herpetofauna) to perform a global assessment of the conserva- tion effectiveness of PAs using species distribution models. Our analyses reveal that >91% of herpetofauna species are currently distributed in PAs, and that this proportion will remain unaltered under future climate change. Indeed, loss of species’ distributional ranges will be lower inside PAs than outside them. Therefore, the proportion of effectively protected species is predicted to increase. However, over 7.8% of species currently occur outside PAs, and large spatial conservation gaps remain, mainly across tropical and subtropical moist broadleaf forests, and across non-high-income countries. We also predict that more than 300 amphibian and 500 reptile species may go extinct under climate change over the course of the ongoing century. Our study highlights the importance of PAs in providing herpetofauna with refuge from climate change, and suggests ways to optimize PAs to better conserve biodiversity worldwide.
... A trait-based approach can also be used to understand the mechanisms of extinction risk (Cardillo et al., 2008). Traits that correlate with extinction vulnerability include low rates of reproduction (Pincheira-Donoso et al., 2021;Purvis et al., 2000) and habitat specialisation (Böhm et al., 2016Isaac, 2009, and if such traits are found in functionally distinctive species and/or in groups of functionally similar species, the loss of FD will be accelerated as such species go extinct. Taken together, these considerations indicate that a functional approach should improve conservation planning for crocodylians. ...
Over half of all crocodylians are threatened with extinction, with many species considered to be functionally extinct throughout their historical ranges. How such losses impact crocodylian functional diversity (FD) and its conservation is poorly understood, but can be investigated using measurable traits. Where such information is unavailable, phylogenetic diversity (PD) has been proposed as an effective strategy to capture FD, but this assumption is not well tested.
We constructed a global trait database for 28 extant crocodylians, and quantified their FD, distinctiveness and groupings. Functionally distinctive crocodylians include the most and least evolutionarily distinct species, likely because unusual trait values and combinations can be produced by both evolutionary isolation and evolutionarily recent adaptive radiation. We identified four functional groups of crocodylians, within which species have similar ecological roles. Highly distinctive species, such as the gharial, fit less well into functional groups.
We combined functional distinctiveness (FUD) and threat ranking scores to prioritise species for conservation. The metric is termed Ecologically Distinct and Globally Endangered (EcoDGE), and we tested how well it operates to preserve crocodylian FD among extant Crocodylia. Under current extinction scenarios, 32%–38% of crocodylian FD might be lost within 100 years. Losses increase to 48% if all threatened species go extinct, with Asia identified as a hotspot of threatened FD in crocodylians. Highly threatened distinctive species lead this extinction scenario, exacerbated by clusters of species sharing traits linked to high extinction risk. These traits include habitat specialism and lower reproductive investment; in contrast, species that tolerate climate extremes are more resilient.
Prioritising at‐risk species based on FUD and threat status appears to be an effective way to conserve present‐day crocodylian diversity. Conservation prioritisation based on the EcoDGE metric performed well to minimise projected losses in FD. Among extant crocodylians, FD losses are projected when high diversity overlaps with high extrinsic threats.
We then examined the utility of PD‐based measures as surrogates for FD conservation, to better understand the advantages and drawbacks of such substitutions. A PD‐based measure such as the Evolutionarily Distinct and Globally Endangered metric provided an effective tool to capture FD in our tests.
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... In recent decades, a stream of global-scale analyses primarily conducted on vertebrates 6,7,15,27-31 -guided by the International Union for Conservation of Nature (IUCN) Red List 23 -have driven considerable progress in determining the quantitative patterns of modern species extinctions through geographic space and across lineages 1,2,6,7 , and the synergies among threats and population features that underlie these patterns 1,2,15,28,29,[32][33][34][35] . Evidence reveals that the geographic and taxonomic distribution of extinctions is heterogeneous, with some regions of the world (e.g., tropical America, Southeast Asia) 1,7,31 and some lineages (e.g., amphibians) 10,15,36 concentrating exceptionally more severe extinction levels than others. ...
The human-induced annihilation of modern biodiversity is dragging the planet into a mass extinction that has already altered patterns of life globally. Among vertebrates, over 500 species have become extinct or possibly extinct in the last five centuries - an extinction rate that would have taken several millennia without human intervention. Vertebrate extinctions have often been quantified as cumulative counts that reveal sharp increases in losses over time. Here, we quantify global tetrapod extinctions since the 1400s using numbers of species losses across successive and independent time periods until present. Our results reveal that extinctions were low and fundamentally restricted to islands in pre-industrial times, experiencing a significant increase and spread over continental mainland following the onset of the industrial revolution. Recent amphibian extinctions alarmingly exceed the extinctions of all tetrapods, while extinctions of island birds account for a third of all extinctions. Finally, we quantified the relationship between human population growth (HPG, as a proxy for aggregate human effects on the environment) and extinctions between 1800-2000, to then predict that an estimated 838 tetrapod species will go extinct between 2030-2100 based on United Nations HPG projections. These findings further warn humanity about the need to sustainably control HPG and the destructive impacts of rapid environmental change on ecosystems worldwide.
... Investment into reproduction is critical for management of energy -whereas patterns of average longevity differ only slightly between amphibians and reptiles, both groups differ considerably in their reproductive activities and outputs. Amphibians (in particular anurans) generally engage in energetically demanding vocal displays to compete over females, and females tend to have much larger clutches than do reptiles (Wells, 2007;Pincheira-Donoso et al., 2021). However, the specific explanation for these observed discrepancies remains difficult to establish at present without risking much speculation. ...
The evolution of brain size is constrained by the trade-off between the energetic costs allocated towards its maintenance and the cognitive advantages that come with a larger brain, leading to a paradox. The cognitive benefits of larger brains (e.g., high behavioural flexibility) mitigate extrinsic mortality factors, which may indirectly select for slower ageing that prolongs lifespan (“cognitive buffer hypothesis”). However, substantial energetic costs imposed by the maintenance of neural tissue is expected to compromise the energetic budget of large-brained organisms, and their investment in somatic maintenance and repair, thus accelerating ageing that shortens lifespan (the “disposable soma theory”). The relationship between lifespan and brain size has mostly been investigated in birds and mammals. Thus, whether these trade-offs express across ectothermic vertebrates remains to be addressed on a large-scale. Our study presents the first large-scale analysis of the brain size-lifespan relationship in ectothermic tetrapods (amphibians and reptiles). Using a dataset spanning 265 species, we performed phylogenetic linear models to investigate the predicted trade-off between variation in brain size and longevity. Our findings revealed a negative relationship between brain size and lifespan across reptiles, whereas no association was observed across amphibians. Thus, the relationship between life history and brain evolution in ectotherms does not follow the general pattern found across other vertebrates. Among ectotherms, the high metabolic cost of producing neural tissue seems to transcend the cognitive benefits of evolving a larger brain. Consequently, our findings suggest that natural selection favours optimization of the energetic economy over the fitness-advantages that cognitive benefits may offer.
... Female investment in reproduction is an energetic expensive component of their life history Healy et al 2019), and within and between egg-laying species, there is substantial variation in reproductive output such as clutch size, clutch numbers, and clutch intervals (Roff, 2002;Shine and Greer, 1991;Pincheira-Donoso and Hunt, 2017;Meiri et al., 2020;Bansal & Thaker, 2021;Fisher et al., 2021;Pincheira-Donoso et al., 2021). Clutch size is the most common reproductive output trait measured and linked to maternal body size, resource availability, and environmental conditions (Lack, 1947;Jetz et al., 2008;Pincheira-Donoso and Hunt, 2017;Meiri et al., 2020;Caracalas et al., 2021). ...
Latitudinal patterns in reproductive output such as clutch size are linked to resource abundance and seasonal climate variation across taxa. Understanding if these patterns hold across local altitudinal gradients and within species can provide insight on key drivers of life-history evolution across scales. In this study, we examined geographical variations in clutch size and climate conditions in a wide-ranging lizard. We collected clutch data from ten populations of E. argus of varying elevation in China from both field observation and from the literature. A total of 369 clutches were obtained and generalized linear mixed-effects models were used to test the relationship between clutch size with body mass, habitat type, elevation, and climate conditions. Body mass strongly correlated with clutch size across all populations. Females from populations at high altitudes with low mean annual temperature and variability, and drier conditions had smaller clutches, while females at lower altitudes with higher mean temperatures and rainfall had larger clutch sizes. Poor climate conditions at high altitudes suggest fewer resources for females to invest in larger clutch size, likely due to reduced foraging and activity times, and growth under unfavourable conditions. These constraints match macroecological patterns of clutch size diversity in egg-laying taxa, suggesting local climate constraints can translate across scales to explain the diversity of reproductive output.
... Although the RL is designed for applied conservation, the standardized assessment across regions and taxa makes it a widely used resource for biogeographic and (macro)ecological research. For instance, RL extinction risk assessments have been used to relate traits, such as body mass, to species extinction risk (Boehm et al., 2016;Pincheira-Donoso et al., 2021;Richards et al., 2021;Rolland & Salamin, 2016), to quantify the effect of threats, such as agriculture, on species extinction risk (Polaina et al., 2018), to quantify links between species extinction risk and invasive species (Tingley et al., 2016;Walsh et al., 2012), to characterize the distribution of threatened species (Coll et al., 2015), to predict future biodiversity losses (Andermann et al., 2021;Monroe et al., 2019) and to understand the potential effects of extinction on large-scale diversity patterns (Oliveira et al., 2020;Smiley et al., 2020). ...
Aim
The Red List (RL) from the International Union for the Conservation of Nature is the most comprehensive global quantification of extinction risk, and widely used in applied conservation as well as in biogeographic and ecological research. Yet, due to the time-consuming assessment process, the RL is biased taxonomically and geographically, which limits its application on large scales, in particular for underdocumented areas such as the tropics, or understudied taxa, such as most plants and invertebrates. Here, we present IUCNN, an R-package implementing deep learning models to predict species RL status from publicly available geographic occurrence records (and other data if available).
Innovation
We implement a user-friendly workflow to train and validate neural network models, and use them to predict species RL status. IUCNN contains specific functions for extinction risk prediction in the RL framework, including a regression-based approach to account for the ordinal nature of RL categories, a Bayesian approach for improved uncertainty quantification and a convolutional neural network to predict species RL status based on their raw geographic occurrences. Most analyses run with few lines of code, not requiring users to have prior experience with neural network models. We demonstrate the use of IUCNN on an empirical dataset of ~14,000 orchid species, for which IUCNN models can predict extinction risk within minutes, while outperforming comparable methods based on species occurrence information.
Main conclusions
IUCNN harnesses innovative methodology to estimate the RL status of large numbers of species. By providing estimates of the number and identity of threatened species in custom geographic or taxonomic datasets, IUCNN enables large-scale automated assessments of the extinction risk of species so far not well represented on the official RL.
... Although the RL is designed for applied conservation, the standardized assessment across regions and taxa make it a valuable and widely-used resource for biogeographic and (macro)ecological research. For instance, RL extinction risk assessments have been used to relate traits, such as body mass, to species extinction risk (Boehm et al., 2016;Pincheira Donoso et al., 2021;Richards et al., 2021;Rolland & Salamin, 2016), to quantify the effect of threats, such as agriculture, on species extinction risk (Polaina et al., 2018), to quantify links between species extinction risk and invasive species (Tingley et al., 2016;Walsh et al., 2012), to characterize the distribution of threatened species (Coll et al., 2015), to predict future biodiversity losses (Andermann et al., 2021;Monroe et al., 2019), and to understand the potential effects of extinction on large-scale diversity patterns (Oliveira et al., 2020;Smiley et al., 2020). ...
Aim: The global Red List (RL) from the International Union for the Conservation of Nature is the most comprehensive global quantification of extinction risk, and widely used in applied conservation as well as in biogeographic and ecological research. Yet, due to the time-consuming assessment process, the RL is biased taxonomically and geographically, which limits its application on large scales, in particular for understudied areas such as the tropics, or understudied taxa, such as most plants and invertebrates. Here we present IUCNN, an R-package implementing deep learning models to predict species RL status from publicly available geographic occurrence records (and other traits if available).
Innovation: We implement a user-friendly workflow to train and validate neural network models, and subsequently use them to predict species RL status. IUCNN contains functions to address specific issues related to the RL framework, including a regression-based approach to account for the ordinal nature of RL categories and class imbalance in the training data, a Bayesian approach for improved uncertainty quantification, and a target accuracy threshold approach that limits predictions to only those species whose RL status can be predicted with high confidence. Most analyses can be run with few lines of code, without prior knowledge of neural network models. We demonstrate the use of IUCNN on an empirical dataset of ~14,000 orchid species, for which IUCNN models can predict extinction risk within minutes, while outperforming comparable methods.
Main conclusions: IUCNN harnesses innovative methodology to estimate the RL status of large numbers of species. By providing estimates of the number and identity of threatened species in custom geographic or taxonomic datasets, IUCNN enables large-scale analyses on the extinction risk of species so far not well represented on the official RL.
Globalisation has accelerated rates of biological invasions worldwide, leading to widespread environmental perturbations that often translate into rapidly expanding socio-economic costs. Although such monetary costs can be estimated from the observed effects of invasions, the pathways that lead invasive species to become economically impactful remain poorly understood. Here, we implement the first global-scale test of the hypothesis that adaptive traits that influence demographic resilience predict economic costs, using invasive terrestrial vertebrates as models given their well-catalogued impacts and characteristics. Our results reveal that total global costs of invasive tetrapods are conservatively in the tens of billions of dollars, with the vast majority due to damage costs from invasive mammals. These monetary impacts are predicted by longevity, female maturation age, diet and invasion pathway traits, although the directionality in the association between impacts and these drivers varied across classes. Alarmingly, costs remain unknown for >90 % of recorded established alien tetrapods worldwide, and across the majority of invaded countries. These huge socio-economic costs demonstrate the necessity of mitigating tetrapod invasions and filling knowledge gaps. Effective identification of traits predictive of costs among and within these groups can facilitate the prioritisation of resources to efficiently target the most damaging existing and emerging invasive tetrapod species.
Pollination underlies the functioning of ecosystems globally. Therefore, the endangerment and extinction of pollinator species are predicted to trigger cascade effects with the potential to alter the demographic collapse of complex ecological networks. However, although some studies have investigated the endangerment levels of pollinator species, the lack of global-scale analyses providing a universal overview of their extinction risks remains a major pending challenge in a world where climate change is rapidly decimating biodiversity. Here, we present the first truly global study of the endangerment level of vertebrate pollinators from across the tree of life. Based on a 1,666 species dataset, we investigate the macroecological patterns of species diversity and extinction risk of bird, mammal, and reptile pollinators of the world. We found higher extinction risk for mammal relative to bird and reptile pollinators. Globally, 1 in 3 mammal pollinators are currently threatened with extinction than 1 in 12 bird and 1 in 8 reptile pollinators. The hotspots of threatened bird pollinators mostly confined to Colombia and Hawaiian Islands, whereas the hotspots of threatened mammal and reptile pollinators are confined to Madagascar and various isolated islands. Notably, the endemic pollinators are more threatened than the widespread pollinators. The increasing decline of population will alter the status of threatened pollinators in future. While highlighting the quantity of threat and decline, we also show that the evolutionary predisposition along with habitat destruction for agriculture, and exploitation for bushmeat and pet trade are combinedly eroding the vertebrate pollinators biodiversity across the world at multiple scales. We suggest special environmental priorities such as controlled land-use, legislation on hunting, collaborative efforts between various stakeholders and community outreach programmes are essential for effective conservation of vertebrate pollinators.
Earth’s old animals are in decline. Despite this, emerging research is revealing the vital contributions of older individuals to cultural transmission, population dynamics, and ecosystem processes and services. Often the largest and most experienced, old individuals are most valued by humans and make important contributions to reproduction, information acquisition and cultural transmission, trophic dynamics, and resistance and resilience to natural and anthropogenic disturbance. These observations contrast with the senescence-focused paradigm of old age that has dominated the literature for over a century yet are consistent with findings from behavioral ecology and life-history theory. Here, we review why the global loss of old individuals can be particularly detrimental to long-lived animals with indeterminate growth, increasing reproductive output with age, and those dependent on migration, sociality and cultural transmission for survival. Longevity conservation is needed to protect the important ecological roles an ecosystem services provided by old animals.
Assessing the extinction risk of species based on the International Union for Conservation of Nature (IUCN) Red List (RL) is key to guiding conservation policies and reducing biodiversity loss. This process is resource demanding, however, and requires continuous updating, which becomes increasingly difficult as new species are added to the RL. Automatic methods, such as comparative analyses used to predict species RL category, can be an efficient alternative to keep assessments up to date. Using amphibians as a study group, we predicted which species are more likely to change their RL category and thus should be prioritized for reassessment. We used species biological traits, environmental variables, and proxies of climate and land‐use change as predictors of RL category. We produced an ensemble prediction of IUCN RL category for each species by combining 4 different model algorithms: cumulative link models, phylogenetic generalized least squares, random forests, and neural networks. By comparing RL categories with the ensemble prediction and accounting for uncertainty among model algorithms, we identified species that should be prioritized for future reassessment based on the mismatch between predicted and observed values. The most important predicting variables across models were species’ range size and spatial configuration of the range, biological traits, climate change, and land‐use change. We compared our proposed prioritization index and the predicted RL changes with independent IUCN RL reassessments and found high performance of both the prioritization and the predicted directionality of changes in RL categories. Ensemble modeling of RL category is a promising tool for prioritizing species for reassessment while accounting for models’ uncertainty. This approach is broadly applicable to all taxa on the IUCN RL and to regional and national assessments and may improve allocation of the limited human and economic resources available to maintain an up‐to‐date IUCN RL.
Reproduction includes two energy investments—the energy in the offspring and the energy expended to make them. The former is well understood, whereas the latter is unquantified but often assumed to be small. Without understanding both investments, the true energy costs of reproduction are unknown. We present a framework for estimating the total energy costs of reproduction by combining data on the energy content of offspring (direct costs) and the metabolic load of bearing them (indirect costs). We find that direct costs typically represent the smaller fraction of the energy expended on reproduction. Mammals pay the highest reproductive costs (excluding lactation), ~90% of which are indirect. Ectotherms expend less on reproduction overall, and live-bearing ectotherms pay higher indirect costs compared with egg-layers. We show that the energy demands of reproduction exceed standard assumptions.
Mesozoic fossils of frogs are rare in the palaeontological record, particularly those exhibiting soft tissues that offer limited insights into early life-history characteristics. Here we report on a skeletally immature frog from the Lower Cretaceous of northwest China, with egg masses in the body and eggs in the oviduct, indicative of a gravid female. CT reconstruction of the specimen allows referral to Gansubatrachus qilianensis and we assign it as a paratype complementing the diagnosis of the type species. The new fossil, which might represent a younger individual than the holotype of Gansubatrachus, shows that sexual maturation occurred before full adulthood in this frog and provides evidence of death linked to mating behaviour. We also discuss other potential sources of variation and life-history traits of Gansubatrachus. The new finding represents the oldest Early Cretaceous frog preserving in situ eggs and provides a glimpse into ancient anuran development during Mesozoic times.
Laterality, the tendency of animals to use the structures on one side of the body more frequently or efficiently than the other side, can reflect the evolutionary history of species, their ecological characteristics, and cognitive abilities. Using anurans as a model system, it has been hypothesized that the strength of laterality (measured as the percentage of right-handed individuals) is higher in terrestrial and arboreal species, which exhibit asynchronous locomotion type (e.g., walking, climbing), than in aquatic species where synchronous locomotion type (e.g., swimming) predominates. We tested these predictions, including body size as an additional factor, in 19 Neotropical anuran species. For this, we obtained data on forelimb use preference for individuals of such species. We then combined these data with published data for another 14 anuran species obtained through a systematic review of the literature. The combined dataset was used to perform a phylogenetic comparative analysis to verify the strength of laterality in the species. We found that four out of the 19 tested species show a percentage of right-handed individuals that was higher or lower than expected by chance. Individuals of these four species exhibit asynchronous movements of forelimbs during displacements, foraging behaviors, sexual displays, or agonistic interactions. Results of a phyloANOVA and a phyloANCOVA indicated that the strength of laterality was higher in species with asynchronous movements, but this was unrelated to microhabitat and body size. Asynchronous (i.e., non-simultaneous) movements of limbs imply alternating muscle contractions and a higher neural asymmetry than synchronous (i.e., simultaneous) movements of limbs. Therefore, species with an asynchronous locomotion type could be reflecting such complexity and neural asymmetry in higher levels of forelimb laterality. Our results mostly support the predictions based on models that cover the expected relationship between the strength of laterality and the evolutionary ecology of vertebrates.
Over recent centuries, invasive species with devastating environmental and socio-economic impacts have rapidly spread worldwide. A hypothesis posits that the number of impactful invasive species increases proportionally with the number of non-native species more generally. A competing hypothesis suggests that certain features (e.g., demographic resilience, ‘fast pace’ life histories) disproportionately enhance the chances of non-native species becoming impactful, causing invasive species to arise disproportionately relative to the numbers of non-native species. However, tests of these hypotheses remain lacking. We develop a null model to test whether invasive species with reported monetary costs reflect global diversities of established non-native species among phyla, classes, and families. Our results reveal that numbers of invasive species with economic costs largely reflect non-native species diversities among taxa (i.e., in 96% of families). However, a few costly taxa were over- and under-represented and their composition differed among environments and regions. Chordates, nematodes, and pathogenic groups tended to be the most over-represented phyla with reported monetary costs, with mammals, insects, fungi, roundworms, and medically-important microorganisms being over-represented classes. Numbers of costly invasive species increased significantly with non-native diversity per taxon, while monetary cost magnitudes at the family level were also significantly related to costly invasive species diversity. Costs were biased towards a few ‘hyper-costly’ taxa (such as termites, mosquitoes, cats, weevils, rodents, ants, and asters). Ordination analysis revealed significant dissimilarity between non-native and costly invasive taxon assemblages. These results highlight taxonomic groups which harbour disproportionately high numbers of costly invasive species and monetary cost magnitudes. Collectively, our findings suggest that effective strategies for mitigation of the rapidly amplifying impacts of invasive species require the prevention of arrival and containment of spread of non-native species as a whole. Yet, the hyper- costly taxa identified here should receive greater focus from managers to reduce impacts of current invasive species.
Aim
Life in mountains is associated with multiple features that increase the risk of demographic collapses in populations – small geographic ranges, short breeding seasons, specialization to harsh climates – leading to the hypothesis that extinction risk is exacerbated in species inhabiting higher elevations. Here, we implement the first test of this hypothesis across the amphibian tree of life – the tetrapods with the largest proportion of montane species, and nature's most threatened animals.
Location
Global.
Time Period
Present.
Major Taxa Studied
Class Amphibia.
Methods
We collated a dataset spanning 8042 species from across all three amphibian orders (Anura, Caudata and Gymnophiona). We preformed phylogenetic logistic regressions to test the predictions that extinction risk increases with elevation, and whether this effect is caused by factors previously hypothesised to drive high‐elevation declines, including restrictions on species' geographic ranges, variation in their life histories and the presence of infectious disease.
Results
Globally, extinction risk increases towards higher elevations. At order‐level, this relationship holds for frogs and salamanders. Even when controlling for geographic range size, life histories and infectious disease, extinction risk increases with elevation for amphibians combined and frogs globally, and in the Americas. In contrast, whereas extinction risk is greater among high‐elevation Eurasian amphibians, this relationship is explained by larger body sizes and lower fecundity.
Main Conclusions
Our analyses indicate that after considering factors previously thought to explain the increase in extinction risk towards higher elevations (e.g., geographic range size, disease), elevation remains a significant predictor of amphibian extinction risk. Given that the only available tests of this hypothesis in other tetrapods (birds and reptiles) conflict with our findings, we suggest that physiological or life‐history features of amphibians may explain this observed phenomenon.
Aim
Species richness varies widely across space and is determined by underlying factors that drive species coexistence. Such factors include the speciation process (sympatric vs. allopatric), time since divergence, geographic context and intrinsic properties of the organisms. We model for the first time the coexistence dynamics of lizards and snakes across broad temporal and spatial scales, investigating whether an increase in niche divergence, dispersal abilities and inhabiting islands or continents affect their probability of coexistence.
Location
Global.
Time period
Cenozoic.
Major taxa studied
Squamata.
Methods
We used 447 sister species pairs, their age since divergence, their level of spatial (sympatric or allopatric) and niche overlap and geographical setting (islands or continents) to fit probabilistic models of species coexistence. We measured morphological traits to quantify niche divergence and used range and body size as proxies for dispersal ability. We applied a model‐comparison framework in lizards and snakes separately to evaluate which factors best explained their coexistence dynamics.
Results
Allopatric speciation is the main speciation mode in snakes but we did not find evidence to favour one speciation mode in lizards. In snakes, sympatric pairs tend to occur on islands and to be more different in body size. On the contrary, dispersal ability shaped the coexistence of lizards, where species were more likely to coexist when they have higher dispersal abilities.
Main conclusions
Distinct patterns and mechanisms underlie species coexistence within the order Squamata. Snake coexistence is preferentially produced by secondary sympatry favoured by niche divergence and is more likely to occur in more restricted geographical settings (islands vs. continents). Coexistence in lizards is strongly influenced only by dispersal abilities, but the high heterogeneity of processes simultaneously shaping the distribution of different lizard lineages might have masked specific coexistence signals, and future work should compare coexistence dynamics between clades (e.g. families).
Biological invasions cause multi-trillion-dollar impacts worldwide. However, the development of approaches to predict drivers and magnitudes of economic costs remain limited. The use of fitness-relevant traits offers a promising, yet neglected, avenue to close this gap. Certain traits acquired during evolutionary history predispose species to succeed in non-native regions and determine variation in impact within and among invasive alien species. Invader’s performance can also rapidly be optimized via natural selection and phenotypic plasticity once exposed to the newly invaded environmental conditions. Given that invader impacts are increasingly viewed through an economic lens, this generates a trait-mediated component of economic impacts that can be quantified through individual traits and the synergistic effects across multiple traits. We discuss these new concepts and highlight emerging transdisciplinary avenues to quantify invasion costs from species traits, and the key roles that big data, museum collections, and machine learning approaches are expected to play.
Aim
The emergence of large‐scale patterns of animal body size is the central expectation of a wide range of (macro)ecological and evolutionary hypotheses. The drivers shaping these patterns include climate (e.g. Bergmann's rule), resource availability (e.g. ‘resource rule’), biogeographic settings and niche partitioning (e.g. adaptive radiation). However, these hypotheses often make opposing predictions about the trajectories of body size evolution. Therefore, whether underlying drivers of body size evolution can be identified remains an open question. Here, we employ the most comprehensive global dataset of body size in amphibians, to address multiple hypotheses that predict patterns of body size evolution based on climatic factors, ecology and biogeographic settings to identify underlying drivers and their generality across lineages.
Location
Global.
Time Period
Present.
Major Taxa Studied
Amphibians.
Methods
Using a global dataset spanning 7270 (>87% of) species of Anura, Caudata and Gymnophiona, we employed phylogenetic Bayesian modelling to test the roles of climate, resource availability, insularity, elevation, habitat use and diel activity on body size.
Results
Only climate and elevation drive body size patterns, and these processes are order‐specific. Seasonality in precipitation and in temperature predict body size clines in anurans, whereas caecilian body size increases with aridity. However, neither of these drivers explained variation in salamander body size. In both anurans and caecilians, size increases with elevational range and with midpoint elevation in caecilians only. No effects of mean temperature, resource abundance, insularity, time of activity or habitat use were found.
Main Conclusions
Precipitation and temperature seasonality are the dominant climatic drivers of body size variation in amphibians overall. Bergmann's rule is consistently rejected, and so are other alternative hypotheses. We suggest that the rationale sustaining existing macroecological rules of body size is unrealistic in amphibians and discuss our findings in the context of the emerging hypothesis that climate change can drive body size shifts.
Variation in genome size spans multiple orders of magnitude among animals. Despite the longstanding debate regarding the adaptive value or costs of genomic complexity, genome size has been proposed to influence extinction risk under the rapidly changing environments of the Anthropocene.
The main hypothesis suggests that genome enlargement increases the accumulation of deleterious mutations while reducing rates of organismal growth and development. These combined effects of larger genome size are predicted to trigger population declines that can lead to extinction, especially under rapidly changing environments that disrupt demographic resilience.
Comparative evidence from terrestrial plants and across vertebrates has provided mixed support for this hypothesis. However, large‐scale comparative studies based on explicit phylogenetic approaches remain lacking. Using a global‐scale amphibian dataset and two recognised proxies of extinction risk (International Union for Conservation of Nature IUCN conservation categories and population trends), we test the prediction that genomes are larger (as estimated by C‐value) in species facing extinction risk. We combine these analyses with life‐history traits widely known to be implicated with extinctions (body size, fecundity), along with a range of environmental factors.
Our phylogenetic analyses consistently failed to identify an effect of genome size on either of the two proxies for extinction risk. The only consistent predictor of extinction risk observed across models performed for amphibians combined and for orders separately was decreasing geographical range size. We also identified a role for larger body size, decreasing range of environmental temperature (for anurans) and increasing levels of UV‐B radiation (for salamanders) as drivers of increasing threat.
Our study provides no support for the prediction that species with larger genomes suffer heightened risk of extinction. We discuss some fundamental limitations underlying the genome size‐extinction hypothesis, and suggest that it is not a promising avenue to elucidate the causes of biodiversity declines in the Anthropocene.
Read the free Plain Language Summary for this article on the Journal blog.
Latitudinal patterns in reproductive output such as clutch size are linked to resource abundance and seasonal climate variation across taxa. Understanding if these patterns hold across local altitudinal gradients and within species can provide insight into key drivers of life-history evolution across scales. In this study, we examined geographical variations in clutch size and climate conditions in a wide-ranging lizard. We collected clutch data from ten populations of E. argus of varying elevation in China from both field observation and from the literature. A total of 369 clutches were obtained and generalized linear mixed-effects models were used to test the relationship between clutch size with body mass, habitat type, elevation, and climate conditions. Body mass strongly correlated with clutch size across all populations. Females from populations at high altitudes with low mean annual temperature and variability, and drier conditions had smaller clutches, while females at lower altitudes with higher mean temperatures and rainfall had larger clutch sizes. Poor climate conditions at high altitudes suggest fewer resources for females to invest in larger clutch sizes, likely due to reduced foraging and activity times, and growth under unfavourable conditions. These constraints match macroecological patterns of clutch size diversity in egg-laying taxa, suggesting local climate constraints can translate across scales to explain the diversity of reproductive output.
A new and extremely small species of the Australopapuan microhylid frog genus Austrochaperina is described on the basis of recently collected material from the base of the Wandammen Peninsula, Cenderawasih Bay, neck of Vogelkop, Papua Province, Indonesia. The description is based mainly on morphological, osteological, and bioacoustic data.
El presente trabajo es un listado de la herpetofauna de los volcanes Popücatépetl e Iztaccihuatl, mismos que se se encuentran ubicados en los límites de los estados de México, Morelos y Puebla. El área de estudio propiamente dicha se encuentra delimitada al este, oeste y parte sur por la cota de 2500 m de altitud y al norte por los 19^ 24’ de latitud norte. Se examinaron 640 herpetozoarios que se encuentran actualmente depositados en la Colección Herpetológica de la Escuela Nacional de Ciencias Biológicas, registrándose además aquellos que cita la bibliografía. Para cada taxón se documentan datos de distribución, descripción morfológica, variación morfométrica y merística de algunas características, así como algunos aspectos biológicos, resaltando notas sobre reproducción y contenidos alimenticios. Se encontró un total de 22 taxa: 9 de anfibios y 13 de reptiles, distribuidos en 77 localidades analizadas. De manera general se establecen posibles relaciones entre la herpetofauna con la altitud y la vegetación. Por último se compara la herpetofauna local con la de otros cinco volcanes del Eje Neovolcánico Transversal (Cofre de Perote, Pico de Orizaba, la Malinche, Nevado de Toluca y Pico Tarrcíntaro). PAlABRAS ClAVE: Herpetofauna. Anfibios, Reptiles, Popocatépetl, Iztaccíhuatl, Biología, Distribución.
Female fecundity is an important selective force leading to female-biased sexual size dimorphism (SSD) in frogs. Because anurans exhibit diverse reproductive modes, we investigated whether variation in SSD and fecundity are related with oviposition site. We asked whether arboreal breeding species show pronounced female-biased SSD and if, paradoxically, females have lower fecundity because of the costs of carrying oocytes and amplectant males. Conversely, we tested whether species that deposit eggs in concealed sites show less
pronounced SSD, because females do not carry males and space limitation may reduce female size and fecundity. Our results showed that, in general, males were approximately 20% smaller than females. However, for species with hidden oviposition sites, males and females exhibited more similar body sizes and arboreal hylids showed more pronounced female-biased SSD. Overall, fecundity was higher in aquatic breeders, as expected, but in hylids, fecundity was smaller in arboreal breeders, which suggests that arboreality may impose restrictions on fecundity. By analysing SSD in a broader and more specific lineage (Hylidae), we found that reproductive microhabitat may also influence female size and fecundity, playing an important role in the evolution of SSD in frogs at different evolutionary scales.
Significance
The ongoing sixth mass extinction may be the most serious environmental threat to the persistence of civilization, because it is irreversible. Thousands of populations of critically endangered vertebrate animal species have been lost in a century, indicating that the sixth mass extinction is human caused and accelerating. The acceleration of the extinction crisis is certain because of the still fast growth in human numbers and consumption rates. In addition, species are links in ecosystems, and, as they fall out, the species they interact with are likely to go also. In the regions where disappearing species are concentrated, regional biodiversity collapses are likely occurring. Our results reemphasize the extreme urgency of taking massive global actions to save humanity’s crucial life-support systems.
While the anthropogenic impact on ecosystems today is evident, it remains unclear if the detrimental effect of hominins on co‐occurring biodiversity is a recent phenomenon or has also been the pattern for earlier hominin species. We test this using the East African carnivore fossil record. We analyse the diversity of carnivores over the last four million years and investigate whether any decline is related to an increase in hominin cognitive capacity, vegetation changes or climatic changes. We find that extinction rates in large carnivores correlate with increased hominin brain size and with vegetation changes, but not with precipitation or temperature changes. While temporal analyses cannot distinguish between the effects of vegetation changes and hominins, we show through spatial analyses of contemporary carnivores in Africa that only hominin causation is plausible. Our results suggest that substantial anthropogenic influence on biodiversity started millions of years earlier than currently assumed. While the anthropogenic impact on ecosystems today is evident, it remains unclear if the detrimental effect of the human lineage on co‐occurring biodiversity is a recent phenomenon or has also been the pattern for earlier hominin species. Focusing on fossil data from East Africa, the cradle of mankind, we find support for a strong negative effect on co‐occurring biodiversity caused by our ancestors already in the Pliocene. Our results suggest that substantial anthropogenic influence on biodiversity started millions of years earlier than currently assumed.
A new small-sized species of dicroglossid frog from West Bengal is described as Minervarya chilapata sp. nov. and compared to Minervarya sahyadris. It differs from all Fejervarya species by its smaller size, by the presence of a distinct white band on upper lip and by the presence of a rictal gland. The new species is separable from its congener in showing a more pointed snout, smaller tympanum and more developed webbing. Its advertisement call is described and compared to that of M. sahyadris. Generic allocation is discussed. In the Fejervarya lineage, a trend towards small-sized species may exist. The species allocated to Minervarya show an important morphological shift, presumably reflecting occupation of a different adaptive niche which might indicate generic distinctiveness.
Three frogs of a new species found in cloud forests on two nearby mountains in Guyana were included in a molecular phylogeny of 17 nuclear and mitochondrial genes (10,739 aligned sites) that revealed that their closest relative is Terrarana (Brachycephalidae, Craugastoridae, Eleutherodactylidae, and Strabomantidae) and their next-closest relative is Hemiphractidae (marsupial frogs). We place these frogs in a new family, genus, and species which is strongly supported as the basal clade within Terrarana: Ceuthomantidae n. fam., Ceuthomantis smaragdinus n. gen, n. sp. Morphological evidence supports the placement of two other species from the Guiana Highlands, Pristimantis aracamuni (BarrioAmorós & Molina) and P. cavernibardus (Myers & Donnelly), in the new family and genus. This close phylogenetic relationship of terraranans and marsupial frogs, nearly all of which have direct development, supports an hypothesis that direct development evolved early in the evolution of this huge clade (~1000 species), for which we propose the unranked taxonomic epithet Orthobatrachia.
We describe three new species of terrestrial frogs of the genus Pristimantis from the province of El Oro, southwestern Ecuador. Two species inhabit the lowland semi-deciduous forests, and the third species in the high montane forests. Pristimantis kuri sp. nov. is characterized by having white patches bordered by dark brown on ventral, inguinal and hidden surfaces of legs, “H” occipito-escapular dermal ridge, and a conical tubercle on the upper eyelid. Pristimantis allpapuyu sp. nov. shows dark brown dorsum with conspicuous cream bands, long and thin digits, and two to three subconical tubercles on the upper eyelid. Pristimantis hampatusami sp. nov. is distinguished by having yellow marks surrounded by brown on groin and posterior surfaces of thighs, and a large subconical tubercle and several small subconical tubercles on the upper eyelid. Describimos tres nuevas especies de ranas terrestres del género Pristimantis de la provincia de El Oro, suroccidente de Ecuador. Dos especies habitan los bosques piemontanos semi-deciduos, y la tercera en los bosques montano altos. Pristimantis kuri sp. nov. se caracteriza por presentar una distintiva coloración ventral, inguinal y de las superficies ocultas de las piernas con sólidas manchas blancas, una cresta dérmica occipitoescapular en forma de “H” y un tubérculo cónico sobre el párpado. Pristimantis allpapuyu sp. nov. tiene una distintiva coloración dorsal café oscura, con conspicuas bandas crema sobre fondo café oscuro en los flancos y muslos, dedos largos y delgados, y dos a tres tubérculos subcónicos sobre el párpado superior. Pristimantis hampatusami sp. nov. se distingue por tener marcas amarillas rodeadas de café rojizo en la ingle y superficies posteriores de los muslos, y un tubérculo subcónico grande y varios subcónicos pequeños sobre el párpado.
A new speeies of Neobatrachus is deseribed from the wheat belt of Western Australia. This species has a diploid karyotype and can be distinguished from congeneric species by morphology and calL Introduction The delineation and identification of species of Neobatrachus has often proved difficult using morphological features alone. The analysis of chromosomes and mating call, however, have facilitated the resolution of species boundaries in this genus (Roberts 1978; Mahony and Robinson 1980; Mahony and Roberts 1986). Having defined species by call and/ or karyotype it has often been possible to find consistent morphological differences between species (e.g. Mahonyand Roberts 1986). During field work in the eastern wheat belt from 1983 to the present we have obtained, from several localities, specimens of a diploid Neobatrachus species which differs in call structure and appearance from N. pelobatoides: the only other diploid species we have observed in this area. These specimens are herein referred to a new species.
Allobates brunneus, long known as Colostethus brunneus, was originally described by E. D. Cope in 1887. Specimens on which the original description was based were collected by H. H. Smith from the village of Chapada dos Guimarães, in the state of Mato Grosso, Brazil. Because of the brevity of the original description, new material of this species was collected from 1998–2001 for a redescription. In recent years, numerous undescribed species of Allobates have been identified throughout the Amazon region. Our redescription of A. brunneus includes many characters not given in the original description that are necessary to distinguish this species from other similar ones. We also include descriptions of the tadpole and vocalization. Allobates brunneus is a small frog, in which males range in snout–vent length from 14.8–18.3 mm, and females from 15.8–19.8 mm. The species typically inhabits swamp forests along small streams or rivers. Although the frog was once abundant, the construction of a hydroelectric dam and reservoir on the Rio Manso has inundated many of the localities where it was formerly known, greatly reducing the number of known populations.
Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’), and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm‐ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g., Classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment‐body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians. This article is protected by copyright. All rights reserved.
The systematics and taxonomy of the polytypic species Craugastor podiciferus are poorly understood due to the high level of phenotypic polymorphism between and within species and the lack of molecular data from topotypic specimens. Herein are reported results of a well-sampled study including all known species of the C. podiciferus species group, several localities from highlands in Costa Rica and western Panama, and for the first time, samples from the type locality of C. podiciferus. A phylogenetic analysis based on the DNA sequences of the mitochondrial 16S rRNA (16S) and cytochrome oxidase 1 (COI) genes and a morphometric analysis are also included. Based on the results, we restrict C. podiciferus to the populations from the Cordillera Volcánica Central and Cordillera de Talamanca in Costa Rica and western Panama. Craugastor podiciferus sensu stricto and six additional clades from the highlands of Costa Rica constitute the well-supported C. podiciferus sensu lato clade. These analyses support the existence of three additional species from the Pacific slope of southwestern Costa Rica and western Panama. Herein, two lineages are described as new species and revised descriptions for C. podiciferus and C. blairi are provided. The name C. blairi is resurrected and used for populations from the Cordillera de Talamanca and Cordillera Central in western Panama. Two additional species are named. One is easily differentiated by the presence of nuptial pads in adult males, a smooth venter, and flat subarticular tubercles. The other, named for populations from southwestern Costa Rica, is recognized by its coarsely areolate venter, projecting subarticular tubercles, and heel without a projecting tubercle. The recognition of these three species from the lower montane rainforest highlights the role of the highlands on the Pacific slope of Costa Rica and Panama in the diversification of the C. podiciferus species group.
A new species of frog, Eleutherodactylus geitonos sp. nov., is described from the southeastern slope of the Cordillera Central, Dominican Republic. The new frog is closely related to E. haitianus and both species share a small size. They differ in some morphological proportions and other external features, coloration, advertisement calls and DNA sequences of the 16S rRNA gene. Morphological and bioacoustic comparisons with other species in the E. abbotti species group are also provided. Our preliminary genetic data suggest that the taxonomic status of E. neodreptus (a synonym of E. audanti) and E. melatrigonum need to be re-evaluated.
We describe three new species of Pristimantis leaflitter frogs from the upper Amazon basin of Ecuador: Pristimantis achuar, Pristimantis altamnis, and Pristimantis kichwarum. Each of these new species was previously considered to be part of a single species, formerly known as Eleutherodactylus ockendeni (Boulenger) morph B. However, analysis of DNA sequences together with examination of the morphology of more than 600 specimens from Ecuador reveals that multiple species were confused under the same name. The morphological differences among the three new species are subtle but consistent: presence or absence of a black canthal stripe and/or supratympanic ridge, snout-vent length, and ventral colouration. The three species are generally allopatric and geographically restricted, although at some localities two of the species occur sympatrically.Describimos tres especies nuevas de ranas del sotobosque de la cuenca Amazónica Ecuatoriana: Pristimantis achuar, Pristimantis altamnis y Pristimantis kichwarum. Estas especies fueron consideradas antes como una sola especie bajo el nombre Eleutherodactylus ockendeni (Boulenger) morfo B. Sin embargo, el análisis de secuencias de ADN y la examinación de la morfología de más que 600 especímenes Ecuatorianos indican que en realidad existen tres especies. Sus diferencias morfológicas son sutiles pero constantes: presencia o ausencia de una raya cantal negra y/o de un pliegue supratimpánico y su coloración ventral. Las tres especies tienen distribuciones alopátricas y distintas aunque en algunas localidades se puede encontrar dos de las tres especies juntas.
We describe a new species of poison frog from central Peru which has been referred to as Ameerega picta and A. hahneli for the past thirty years. To our knowledge the new species is endemic to Peru and occurs throughout the east-Andean versant between roughly 6 and 10 degrees south latitude. Recent phylogenies using molecular data show that the new species and A. hahneli are not closely related despite being similar in pattern, color, and morphology. Our data suggest that the new species is a sister taxon to A. rubriventris, which is readily distinguishable from the new species by its reddish venter. The new species can be distinguished furthermore from other Ameerega species by possessing white (rather than yellow or cream) dorsolateral stripes, and from the similar A. hahneli by differences in advertisement calls and larval morphology.
Body size and age structures of two breeding populations of Rana tagoi tagoi were studied in southwestern Kanto. The mean snout-vent length of males and females was 42.2 and 44.2mm in Kanagawa, and 41.7 and 42.2mm in Tokyo, respectively. The populations studied exhibited almost no sexual dimorphism in body size. Rana. t. tagoi was successfully aged by skeletochronology using phalanges. The breeding adults were 2-4yr old and the age at first reproduction was estimated to be 2-3yr. Their lifetime growth schedule was also estimated, based on the relationship between body size and age.
The Viva Natura: Field Guide to the Amphibians, Reptiles, Birds and Mammals of Western Mexico is the first publication of its kind written about the fauna of this region. The purpose of the field guide is to introduce the reader to the wealth of amphibians, reptiles, birds and mammals of Western Mexico and help identify them in the field. This guide contains the vast majority of the conspicuous animals of the region. In this second edition there are 230 species in this guide and a total of 440 full-color photos. The guide is extremely easy to use. The book is completely bilingual (English and Spanish). The book commences with a brief introduction to the study area, its geography, climate and ecosystems. Chapters dedicated to the four groups of fauna (amphibians, reptiles, birds and mammals) follow. Each chapter begins with an introduction followed by photographic plates that depict conspicuous species of the study area. All photos were taken by the author himself and with few exceptions, show animals in their natural habitat under completely natural conditions. Each species is described by both its common and scientific names and also by a set of icons that illustrate the species characteristics, such as its habits, diet, preferred habitat, protection status, ect. Color bands on the outer edge of each species plate indicate one of the three principal habitat types (Ocean, Coast and Islands, Freshwater, Forest and Gardens) where this particular species can be observed most frequently. Silhouette thumbs on the plates edges portray a typical member of each group of fauna, making browsing the guide more efficient. The final chapter of the book is dedicated to the conservation issues inside the study area. The book is supported by a companion website where additional texts, photos and also videos and sounds can be found.
Aim
Body size explains most of the variation in fitness within animal populations and is therefore under constant selection from ecological and reproductive pressures, which often promote its evolution in sex‐specific directions, leading to sexual size dimorphism (SSD). Several hypotheses have been proposed to explain the vast diversity of SSD across species. These hypotheses emphasize: (a) the mate competition benefits to larger male size (sexual selection); (b) the benefits of larger female size for fecundity (fecundity selection); (c) the simultaneous benefits of niche divergence for males and females to reduce intersexual competition for ecological resources (natural selection); and (d) the underlying impact of geographical variation in climatic pressures expected to shape large‐scale patterns of SSD in synergy with the above selection pressures (e.g., intensification of fecundity selection as breeding seasons shorten). Based on a new, global‐scale amphibian dataset, we address the shortage of large‐scale, integrative tests of these four hypotheses.
Location
Global.
Time period
Extant.
Major taxa studied
Class Amphibia.
Methods
Using a > 3,500 species dataset spanning body size, ecological, life‐history, geographical and climatic data, we performed phylogenetic linear models to address the sexual, fecundity, ecological and climatic hypotheses of SSD.
Results
Evolution of SSD is discordant between anurans and salamanders. Anuran SSD is shaped by climate (male‐biased SSD increases with temperature seasonality) and by nesting site. In salamanders, SSD converges across species that occupy the same types of microhabitats (“ecodimorphs”), whereas reproductive or climatic pressures have no effects on their SSD. These contrasts are associated with latitudinal gradients of SSD in anurans, but not in salamanders.
Main conclusions
Amphibian SSD is driven by ecological and climatic pressures, whereas no roles for sexual or fecundity selection were detected. We show that macroevolutionary processes determined by different forms of selection lead to latitudinal patterns of trait diversity, and the lack of them.
Aim
Clutch size is a key life‐history trait. In lizards, it ranges over two orders of magnitude. The global drivers of spatial and phylogenetic variation in clutch have been extensively studied in birds, but such tests in other organisms are lacking. To test the generality of latitudinal gradients in clutch size, and their putative drivers, we present the first global‐scale analysis of clutch sizes across lizard taxa.
Location
Global.
Time period
Recent.
Major taxa studied
Lizards (Reptilia, Squamata, Sauria).
Methods
We analysed clutch‐size data for over 3,900 lizard species, using phylogenetic generalized least‐square regression to study the relationships between clutch sizes and environmental (temperature, precipitation, seasonality, primary productivity, insularity) and ecological factors (body mass, insularity, activity times, and microhabitat use).
Results
Larger clutches are laid at higher latitudes and in more productive and seasonal environments. Insular taxa lay smaller clutches on average. Temperature and precipitation per se are unrelated to clutch sizes. In Africa, patterns differ from those on other continents. Lineages laying small fixed clutches are restricted to low latitudes.
Main conclusions
We suggest that the constraint imposed by a short activity season, coupled with abundant resources, is the main driver of large‐clutch evolution at high latitudes and in highly seasonal regions. We hypothesize that such conditions – which are unsuitable for species constrained to laying multiple small clutches – may limit the distribution of fixed‐clutch taxa.
Age at sexual maturity is a central life-history parameter, strongly related to key traits such as body size and longevity.
It is influenced by environmental and intrinsic factors that affect growth rates and gonad development. Using
data on the age at sexual maturity in 123 species of amphibians worldwide, we tested whether sexual maturity is
delayed at high altitudes and latitudes, in cold and dry regions and on islands. We further tested whether sexual maturity
is delayed in species with parental care and direct development (no tadpole stage). Using phylogenetic regression
and correcting for body size, we found a positive relationship between latitude and sexual maturity. Surprisingly,
altitude was negatively correlated with sexual maturity in small species. Temperature was negatively related to
sexual maturity in females but not in males. Precipitation and seasonality did not effect on either sex. Species that
engage in parental care or have direct-developing larvae mature early. We found no effect of insularity, contradicting
the insular syndrome hypothesis. Meta-analyses revealed that, within species, sexual maturity is reached at younger
ages in warm temperatures in aseasonal environments and in low altitudes. Thus, although life-history strategies
affect maturation time, climate can further delay or accelerate development – probably through effects on metabolic
rates and season length.
Throughout much of the world, frog populations are declining, with the survival of many species under threat. In Australia, several species have become extinct in the past 35 years. This second edition of Field Guide to the Frogs of Australia provides fully updated accounts of all the known frogs of Australia. There are 248 species within the five native frog families: Hylidae, Limnodynastidae, Microhylidae, Myobatrachidae and Ranidae. Also included are the introduced Cane Toad and nine ‘stowaway’ species that have arrived in Australia. Each species account includes details of size, status, distribution, habitat, behaviour and advertisement call. Species are beautifully illustrated with full-colour paintings and distribution maps are also included. Closely related frogs are shown in identical poses so that comparisons can be made readily. The introductory section of the book covers frog biology and habitats and includes notes on families and genera.
We describe a new species of Ranitomeya (family Dendrobatidae) which we discovered on a recent expedition to the Río Apaporis region in southeastern Colombia. This species had previously been referred to as Dendrobates quinquevittatus sensu Silverstone, based on a single specimen collected in the 1950s from the mouth of Río Apaporis. We found additional specimens from two sites in this region; near the town of La Pedrera (Departamento Amazonas), and on the lower Apaporis (Departamento Vaupés). We also found several R. ventrimaculata, and the two species are likely sympatric throughout much of this region. Although the new species and R. ventrimaculata have similar life-history attributes (such as using similar bromeliads for tadpole deposition), the two species clearly differ in color pattern and advertisement call parameters. Ongoing molecular studies indicate that the new species is not closely related to the sympatric R. ventrimaculata, but rather is sister to an apparently undescribed species of Ranitomeya from the upper Brazilian Amazon.
Three new species of rainfrogs of the genus Pristimantis are described from a large mesa (tepui), the Wokomung Massif, of the Pakaraima Mountains in west-central Guyana. Pristimantis dendrobatoides n. sp. is known from 1385–1411 m, P. jester n. sp. from 1411–1650 m, and P. saltissimus n. sp. from 698–1560 m elevation. The three species are syntopic at elevations around 1400 m in cloud forest. All three taxa are unusual among species of Pristimantis in the production of malodorous and distasteful skin secretions when handled, conditions that are atypical for the genus. Two of the new species (P. dendrobatoides, P. jester) also have bright, red skin coloration, and the third (P. saltissimus) is either cryptically colored or brightly colored.
A new species of Aparasphenodon is described from patches of arboreal restinga within the Atlantic Forest Biome, in a region known as Baixo Sul in southern Bahia, northeastern Brazil. Aparasphenodon arapapa sp. nov. is promptly diagnosed from other Aparasphenodon mainly by having small size (male snout-vent length 57.4–58.1 mm), loreal region flattened and wide, and canthus rostralis rounded and poorly elevated. The wide and flattened snout resembles that found in Triprion and Diaglena, and possibly is a parallelism (homoplasy) related to the phragmotic behavior of casque-headed tree frogs to their microhabitat usage. The decision to allocate the new species in the genus Aparasphenodon is discussed in detail, as the single morphological synapomorphy of the genus, the presence of a prenasal bone, is insufficient to morphologically relate the new species to Aparasphenodon, Triprion, or Diaglena.
We describe three new species of poison frogs discovered on recent expeditions throughout Central Peru. Two of these were discovered from the Serranía de Contamana, a small mountain range near the town of Contamana on the Río Ucayali in Central Peru. The first of these species is similar in appearance to Ameerega petersi, but the two species differ in call and size, have allopatric distributions, and are not close relatives according to a Bayesian phylogeny. This species is also similar morphologically to A. pongoensis, although the latter lacks flash marks above the groin and has a distinct advertisement call. Our phylogenetic data suggest that this species is closely related to A. bassleri, a species which is much larger and usually possesses a brightly-colored yellow or orange dorsum. The second new species has a red dorsum and is similar in appearance to A. bassleri, A. cainarachi, and the third new species described herein, but can be distinguished by its unusual advertisement call. The third new species in this paper was discovered in the upper Huallaga Valley near the towns of Tocache and Juanjui. This species resembles certain populations of A. bassleri and the second new species (mentioned above), but can be diagnosed by its advertisement call which is significantly slower than its closest relatives; approximately one-half the speed of A. bassleri and one-quarter the speed of the second new species. Finally, we discuss the biogeography of the A. bassleri clade in light of these new discoveries. The biogeography of this clade is consistent with the disturbance-vicariance hypothesis, and climatic fluctuations were likely a major driver in the divergence and speciation of this group. We also present a phylogeny with increased sampling in the A. petersi clade and discuss the taxonomy of the group.
We describe three new species of the plethodontid salamander genus Oedipina from Honduras. All three are relatively small to moderate sized, elongated and attenuate forms, which are differentiated from each other and from other members of the genus in limb and digital features, size, and body shape. Their distinctiveness is validated by phylogenetic analysis of mtDNA (cytochrome b and 16S) data, which shows each to be strongly differentiated. Furthermore, two of the three species are sister taxa and they comprise a third major clade in the genus, which we recognize as a new subgenus.
Oreobates barituensis sp. nov. is described from the ecoregion of southern Andean Yungas forests of north-western Argentina at elevations of 1100 to 1300 m above see level. It shares morphological characters with the sympatric and syntopic O. discoidalis, as well as with O. ibischi and O. cruralis from Bolivia. The recognition of the new species is in particular supported by considerable differences in the advertisement call among these species. We also made some considerations on probable conspecificity of northern Argentina and Bolivian populations of O. discoidalis and O. cf. cruralis.
We describe two new species of forest frogs in the genus Platymantis from the Isabel Island group, Solomon Islands. One new species is a medium-sized, terrestrial form that is morphologically most similar to P. weberi (a widespread Solomon Islands species). The other new species is an arboreal frog that is morphologically similar to Platymantis neckeri (known from Bougainville, Choiseul, and Isabel islands). Both new species possess unique advertisement calls that distinguish them from all sympatric congeners. Because acoustic characteristics function as the primary mate-recognition signals for anuran species, and are therefore an excellent indicator of the status of unique evolutionary lineages, we recognize each as new species. We diagnose both new species on the basis of their distinctive advertisement calls and in the case of the terrestrial form, by differences in body size, body proportions and skin texture. The diversity of ceratobatrachid frogs of the Solomon islands and Bougainville is underestimated and in need of a comprehensive taxonomic review coupled with a standardized survey of acoustic characters.
A new species of the dicroglossine genus Limnonectes from eastern Thailand and its tadpole are described. Analysis of DNA sequence data from 2518 base-pairs of the mitochondrial 12S and 16S gene regions places the species within the complex of frogs currently referred to as Limnonectes kuhlii and demonstrates it to be a separate lineage (>18% sequence divergence from type-material of L. kuhlii from Java). The new species differs from L. kuhlii by having nuptial pads, a greater snout–vent length, and different relative finger lengths than specimens from Java. It has more extensive toe webbing, a different arrangement of nuptial pads, and a greater snout–vent length than Limnonectes laticeps. The new species, which lacks vocal slits, also can be distinguished from the morphologically similar Limnonectes namiyei from Japan, which possesses vocal slits.
A new arboreal species of the Chaunus veraguensis group is described for the humid montane forest of Madidi National Park, in northern Bolivia. The new species differs from other species in the group by the combination small size, long and slender extremities, webbed hands, conspicuous tympanic membrane, well developed parotoid glands, absence of large glands on dorsum and extremities, nuptial excrescences of males composed of pungent spines on dorsal surface of thumb, greenish-brown coloration on dorsum with red warts in life, and green iris. It is only known from two nearby localities in the Serranía Eslabón, Department La Paz. An operational key for species in the C. veraguensis group is provided.
