Global Assessment of Reptile Distributions
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Exploring drivers of viviparity amongst global reptiles

5/10/2022

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Picture Top: Cerastes vipera (a live-bearing viperid snake); bottom: Cerastes cerastes (an egg-laying congener). (Photo: Anna Zimin)
In a recent publication in Global Ecology and Biogeography we (Anna and many others) examined the selective forces that potentially drive the evolution of viviparity (live-bearing) in squamates.
Vertebrates are known for their versatility in reproductive strategies and features. Those, in turn, facilitated their successful expansion across various types of environments worldwide. For instance, the evolution of shelled eggs promoted the expansion of tetrapods into terrestrial habitats, and the retention of eggs inside the parent’s body significantly improved embryo survivability in harsh environmental conditions. Live-bearing (henceforth ‘viviparity’) evolved across all major vertebrate groups, except birds, crocodilians and turtles. Whereas it evolved only once in the mammal history, it is thought to evolve over 100 times independently in squamates (lizards and snakes), with about 20% of their species being viviparous. The prevalence of both egg-laying (oviparity) and viviparity in many squamate clades, and the multiple origins of viviparity, make squamates an excellent model to study the selective forces behind the evolution and biogeography of reproductive modes.
In this study, we aimed to examine most of the common selective forces hypothesized to drive the evolution of viviparity, and the relationship of reproductive mode with body size. Specifically, we tested the predictions that viviparity will be associated with (1) cold climates, (2) unpredictable climates, (3) high elevations (a proxy for hypoxic conditions), and (4) large adult body sizes. In order to do that, we collated a dataset for over 9,000 squamate species (about 80% of non-marine living species), making it the largest-scale study on the subject. Furthermore, because the factors mentioned above may be associated both directly and indirectly (i.e., through another factor) with reproductive mode, we used methods, such as path analysis, that enable to detect and account for such complex relationships.
Our main finding was that viviparity was strongly associated with cold climates, in line with earlier studies. In fact, there are relatively more viviparous than oviparous species in colder climates, and some of the coldest regions occupied by squamates do not include oviparous species at all. Notably, although some warm regions harbor many viviparous species (much more than the coldest climates), such regions usually include even more egg-laying species. The roles of climatic variation and of elevation were found to be less important and not straightforward. Even though the proportions of viviparity at high elevations are higher, elevation probably exerts various selective pressures and influences the prevalence of viviparity primarily through its effect on temperature. Our findings highlight the complexity of processes potentially underlying the evolution of viviparity, but they also provide clear support for low temperatures as selecting for viviparity in squamates.

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Top left: Global richness of viviparous squamate species. Top right: latitudinal variation in richness of viviparous squamate species. Bottom left: Proportion of viviparous squamate species in grid cells. Bottom right: latitudinal variation in proportion of viviparous squamate species.
Author: Anna Zimin
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Modelling IUCN threat status for global reptiles

1/5/2022

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PictureVallarta Mud Turtle (Kinosternon vogti), classified as ‘Critically Endangered’ by the automated assessment method and as not evaluated by the IUCN Red List of Threatened Species (Photo: Agencia Informativa Conacyt/ Wikimedia)
Reptiles comprise nearly 11,800 species worldwide, and are the most species-rich land-vertebrate group. After 18 years of laborious work by many experts globally, early in 2022, the first extinction risk assessment of this group was completed (the Global Reptile Assessment). This important endeavor will enable adding reptiles to global conservation policy and management initiatives as one of the major groups assessed. Nevertheless, this assessment still leaves over 3000 reptile species that have either not been assessed or were assigned a data deficient category that prevents their prioritization for conservation. In an effort to fill-in this gap a new publication in the journal PLOS Biology, we presents estimates of extinction risk for those species currently neglected by the Global Reptile Assessment, using novel machine learning modelling. importantly we found that unassessed and data deficient reptile species are more likely to threatened than assessed species.
Gabriel Caetano, lead author of the paper explained “The IUCN threat assessment procedure is highly important, yet very lengthy, data intensive, subject to human decision biases, and relies on in-person meetings of experts. However, we can use information on already assessed species to better understand the risks to those not yet assessed. Species may share physiological, geographic, and ecological attributes (often via shared evolutionary history) that make them more threatened, and experience similar sources of threat when they occur at similar locations. In our work we tried to emulate the IUCN process using predominantly remotely sensed data and advanced machine learning methods. We used species that have been assessed to teach our models what makes a species threatened and then predict the threat categories of unassessed species”. He added “our new methods are important for highlighting reptile species at risk and can be used on other groups as an initial shortcut for threat categorization”.
Shai Meiri added “Importantly, the additional reptile species identified as threatened by our models are not distributed randomly across the globe or the reptilian evolutionary tree. Our added information highlights that there are more reptile species in peril – especially in Australia, Madagascar, and the Amazon basin – all of which have a high diversity of reptiles and should be targeted for extra conservation effort. Moreover, species rich groups, such as geckos and elapids (cobras, mambas, coral snakes, and others), are probably more threatened than the Global Reptile Assessment currently highlights, these groups should also be the focus of more conservation attention”
Uri Roll mentioned “Our work could be very important in helping the global efforts to prioritize the conservation of species at risk – for example using the IUCN red-list mechanism. Our world is facing a biodiversity crisis, and severe man-made changes to ecosystems and species, yet funds allocated for conservation are very limited. Consequently, it is key that we use these limited funds where they could provide the greatest benefits. Advanced tools- such as those we have employed here, together with accumulating data, could greatly cut the time and cost needed to assess extinction risk, and thus pave the way for more informed conservation decision making”.

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Proportion of reptile species in different threat categories for an Automated Assessment Method and for the IUCN Red List of Threatened Species.
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Between a rock and a hard place – unique rare species face grave dangers due to human action

24/11/2021

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In a recent paper published in the journal Science Advances Gopal explored drivers of phylogenetically endemic land vertebrates. He also looked at conservation attributes of regions with high phylogenetically endemic species.

We live in the age of the ‘sixth mass extinction’. Our daily activities are causing hundreds and thousands of species to be lost forever. To turn the tide on the biodiversity crisis we have to identify those regions and species that are most in need of our conservation efforts. However, the characteristics of regions or species most in need of protection are not always clear. In this work we focus on those species that have two distinct features that make especially good candidates for conservation efforts. First – they are confined to only small and distinct location on the globe – what are known as endemic species and face greater risk of extinction. Second – they are evolutionary unique - they do not have close relatives on the ‘tree of life’ and their loss will represent a loss of millions of years of evolution. Species that poses both of these attributes (phylogenetic endemics) are therefore of great conservation importance as they represent unique and threatened components of biodiversity. To explore these species, we collected data regarding the evolutionary relationships and geographic distribution of almost all land vertebrate species (~30,000 species of amphibians, birds, mammals, and reptiles). We set out to map global ‘hotpots’ of such species, understand what are the unique conditions that support them, and evaluate their current protection and threats.
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Some of the range-restricted evolutionary unique species. The Red ruffed lemur (photo credit: Charles J Sharp), Madagascar fish eagle (photo credit: Anjajavy le Lodge), Hula painted frog (photo credit: Gopal Murali - own image), and Chinese Crocodile Lizard (photo credit: Holger Krisp). Images from Wikimedia Commons (apart from the painted frog).

We found that hotspots of phylogenetically endemic species mostly occur in the tropics and in the southern hemisphere along mountain ranges and in islands. Altogether, these hotspots, when combining the hotspots for all of the four above-mentioned groups, they occupy 22% of the total landmass. Hotspots that were important for all of the four groups are located in the Caribbean islands, Central America, along the Andes, eastern Madagascar, Sri Lanka, southern Western Ghats in India, and New Guinea. Although some of these regions have been previously prioritized for conservation actions, our study also found hotspots outside well-known biodiversity centres. For instance, we found the Asir mountains in Saudi Arabia to be important for such unique birds and Morocco to harbour phylogenetically endemic reptiles. Globally, these regions are mostly defined as mountainous tropical regions. This finding supports the notion that tropical mountains have an important role in the generation and maintenance of biodiversity.

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Global map of Phylogenetic endemism hotspots for all land vertebrates corrected for species richness

We next quantified how human activities and climate change are threatening these hotspots. Alarmingly, we found human activities such as buildings, roads, land-use, population density, and rate of climate change to be disproportionately higher in these hotspots (when compared to regions outside them). Consequently, our study highlights that many uniquely rare species, which probably perform important roles in the ecosystem, will be the first to be lost due to global change. Furthermore, we found most of the hotspots are not adequately protected. About 70% of the hotspots regions have less than 10% overlap with protected areas. Some of these regions which require urgent conservation action are the southern Andes, Horn of Africa, Southern Africa, and the Solomon Islands.
 
To-date most conservation strategies still focus on species-rich regions or flagship species, which may miss out on regions with uniquely rare species we identified. Overall, our study emphasizes on the need for strategic conservation policy and management to safeguard the persistence of thousands of small-ranged species that represent millions of years of unique evolutionary history.

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Infographic representing this work. Press to download in high resolution
Author: Gopal Murali
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Here be dragons; but why? The biogeography and evolution of Melanesian forest dragons (Agamidae)

9/2/2020

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PictureHypsilurus papuensis (Photo Oliver Tallowin)
Australia and New Guinea, collectively referred to as the Sahul, share many biotic elements; but could not be more different in terms of climate and geological history. Australia as a landmass is relatively geologically stable, does not have much in the way of mountains and is predominantly covered in arid deserts. In contrast, New Guinea is relatively young in geological terms, has extensive mountains ranges across the entire island and is largely covered in tropical rainforests. From a biogeographical perspective these landmasses present very different opportunities and challenges to their prospective biotic assemblages, and yet, there are some lineages that have diversified throughout both regions. Agamids, also referred to as ‘dragons’, have proliferated in arid Australia represented by over 100 species and have been relatively well studied. With 20 recognised species, Melanesian agamids are much less diverse, have received much less scientific attention, and yet have been shown to be closely related to the Australian clade. In a paper published in the Biological Journal of the Linnean Society, we examine the evolution, biogeography and ecological diversity of Melanesian agamids. We tested whether they originated on the Australian Craton or proto-Papuan islands to the north. Also, we examined to what extent mountains have played a role in Melanesian agamid diversification and tested the evolutionary trends and origins of agamid ecological diversity.

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α-Diversity of agamids across Australia, New Guinea and surrounding islands
PictureLophosaurus dilophus (Photo Oliver Tallowin)
In addition to the 11 recognised Melanesian agamids sampled, we found further monophyletic divergent lineages in four taxa. This included two lineages within Hypsilurus modestus, and three within H. magnus, H. papuensis and Lophosaurus dilophus. We found little evidence for micro-endemism in Melanesia with most taxa being widespread and low genetic divergence across the Central Cordillera suggesting these mountains have only recently become a barrier to dispersal. We identified clear evidence of past over-water dispersal in Hypsilurus agamids, with H. modestus lineages dispersing between New Britain, New Ireland and northeast New Guinea. Also, the restricted range of H. schoedei and disjunct distribution of H. longii indicates insular extinction events may have occurred. We identify the Australian Craton as the ancestral area of Lophosaurus and all Australo-Papuan agamids. However, Hypsilurus were clearly able to disperse over water and show deep divergences in the Melanesia region. The distribution of extant Hypsilurus lineages suggests a history of allopatric speciation on former islands with some now accreted onto New Guinea. We infer from the biome evolution analysis that Australo-Papuan agamids were associated with rainforests which date back to the early Miocene, but also that agamids had similarly long histories in other biomes. This indicates that while the rainforest biome might well be ancestral for many Australian radiations, semi-arid or seasonal environments also have a long history in Sahul. Finally, we note the disparity in ecological diversity within Australo-Papuan agamids. Despite their long history in rainforest regions there is a complete lack of Melanesian terrestrial or semi-terrestrial agamids compared with the Australian assemblage. This reflects fundamental differences in how these lizards diversify in dry versus wet habitats and suggests adverse environmental conditions, such as reduced solar radiation, as well as biotic interactions, such as competition or predation, form a barrier to ecological diversification in rainforest biomes.

Author: Oliver Tallowin
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Unraveling evolutionary trends in New Guinean geckos

9/2/2020

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Uncovering the evolutionary trajectories of species assemblages can provide fascinating insights into the past environmental and geological processes, as well as the biological traits, that have led to present day diversity patterns. Furthermore, time-calibrated phylogenies can shed light on the historical sequence and timing of speciation events which, in turn, can be used to complement geological models aimed at reconstructing the formation of the earth. In our paper published in Molecular Phylogenetics and Evolution, we focus on the Melanesian radiation of bent-toed geckos (Cyrtodactylus), a clade occurring throughout New Guinea and adjacent islands, and Australia’s tropical northeast. We examine the sequence and timing of diversification in Australo-Papuan Cyrtodactylus and investigated three biogeographic scenarios. Firstly, did Cyrtodactylus diversification originate on the Australian Craton or former proto-Papuan islands to the north. Secondly, does Australo-Papuan Cyrtodactylus diversity correlate with distinct geological regions and to what degree do they exhibit infra-regional clustering. Lastly, to what extent did New Guinea mountain uplift impact Cyrtodactylus diversification and if so when did this occur.
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Cyrtodactylus serratus (Photo S. Richards)
We found that in addition to 28 recognised Australo-Papuan Cyrtodactylus species, there were ten distinct lineages that we consider candidate species. Our ancestral-state analyses support the early origin and diversification of Australo-Papuan Cyrtodactylus on the proto-Papuan islands, and indicate that once insular lineages arrived to New Guinea following the accretion of their associate island onto the mainland’s northern margin. We found a high degree of phylogenetic clustering within the regions and found compelling evidence that the East-Papuan Composite Terrane (or south-eastern Papuan Peninsula) has played a long-term important role in the accumulation of New Guinean Cyrtodactylus. Finally, we identified that the Late-Miocene uplift of New Guineas Central Cordillera was responsible for isolating north-south lineages and mediated the accumulation of diversity in a manner consistent with that observed in other tropical mountain regions.

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Cyrtodactylus epiroticus (Photo Oliver Tallowin)
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Geographic distribution of each of the nine major lineages are illustrated with corresponding colors on the two maps, and specimen representatives of each lineage shown on the right.
Author: Oliver Tallowin
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Lizard archetypes: the seven forms of saurian ecology

28/7/2019

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We tend to think of ways to categorize animals either by shape (4 legs? 2 legs? no legs?, thin? Fat? big headed? small headed?) or phylogenetic affinities (reptiles? lesser animals? Snakes? Skinks?). But what about ecology?
The many aspects of a species ecological niche are generally quantified singly, or we refer to some abstract “multidimensional niche”, meaning we give up trying to characterize it before we even started. In a paper published recently in the Journal of Biogeography GARDians, led by Enav Vidan and Jonathan Belmaker, tried to define, and numerate, the main types of lizards out there – as reflected in their ecology.

PictureKomodo dragon (Photo: Marinus Hoogmoed)
We have selected four traits that we felt define much of the fundamental axes of ecological variation seen in lizards: 1. use of space / microhabitat preference, that defines where in the environment a lizard is active (on the ground? In trees or rocks? Under ground? In water?); 2. Activity times: species active in the same place, or even on the same branch or piece of ground, can segregate their use of the environment by dividing the temporal niche. Furthermore, being diurnal or nocturnal (or being cathemeral and enjoy both ‘worlds’) has strong implication on thermal biology and hence on metabolism and rates in which lizards take up resources and exchange them with the environment; 3. Diet: is a species insectivorous/carnivorous, as most lizards are? Or do they predominantly feed on plant matter (these guys seem to even take more leaves and plant parts with lower energy content)? Or do they in fact use both plants and animals (and then probably energy richer plant parts such as berries or sap)? This is directly related to the way a lizard affects its environment and may also influence its position across the sit and wait-active foraging continuum (no use waiting for plants); 4. Body size – while not an ecological trait per se size nonetheless strongly influences a host of ecological processes, from the degrees of metabolism and energy flow, to the types of available foods – and potential predators.
These four traits obviously interact, and some combinations may be more or less common than others: small, diurnal, terrestrial insectivore is after all the first picture to pop to mind when the term ‘lizard’ is introduced (except for the diehard gecko lovers among us, and well, there are a few of us with this infatuation). But are there tiny nocturnal herbivores? Or huge nocturnal lizards? How common is a marine iguana  (large, herbivorous, swimming diurnal beast) type lizard – do we remember it simply because it is exotic?

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Functional diversity of Lizards as a function of species richness
PictureStenodactylus petrii (photo: Marco Ferrante)
We used Archetypal Analysis to assign lizards to types – or archetypes. Archetypal Analysis is an unsupervised machine learning technique that seeks to find the number of clusters that create the smallest convex hull in an n-dimensional trait space, by using the extreme values rather than the centroid of the clusters. AA assigns, for each species, a vector of affinities to each archetype. Most species are probabilistically assigned to several archetypes, with the partial probabilities summing to one.
We found that the most common functional trait combinations are (1) diurnal, terrestrial, carnivores (20% of the species); (2) diurnal, scansorial, carnivores (16%); and (3) nocturnal, scansorial, carnivores (13%).
Lizards could be robustly classified into seven ecological “Archetypes”:
  1. terrestrial (obviously, usually small, carnivorous, diurnal thing that are, well, active on the ground), think Ablepharus skinks, for example
  2. Scansorial – small diurnal, carnivorous, scansorial species, such as Pristurus rupestris.
  3. Nocturnal – small terrestrial, scansorial and carnivorous species that are, at least partially, active at night (i.e. they are either nocturnal or cathemeral). Like most geckos of course – say Hemidactylus
  4. Herbivorous - relatively large, diurnal, terrestrial and scansorial species whose diet includes substantial amounts of plant matter (either as omnivores or herbivores). Saharo-Arabian Uromastyx for example fit the bill very nicely
  5. Fossorial – lizards living at least partially underground, mainly small, carnivorous, with varied activity times. Many skinks, such as Ophiomorus represent this strategy
  6. Large - very big (all species >200 g), mainly diurnal, terrestrial or scansorial species. You know, Varanus komodoensis and Komodo-dragon wannabes.
  7. Semi-aquatic - dwelling in aquatic habitats, relatively large, and generally both carnivorous and diurnal, things like Uranoscodon superciliosus

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PictureUromastyx ornata (photo: Alex Slavenko)
We then partitioned the global spatial patterns of lizard richness into these seven archetypes, and found that each shows pretty distinct patterns. Turns out Australia is the main hotspot for the herbivorous, nocturnal, fossorial, and terrestrial strategies – and for lizards in general. The Amazon basin is the main hotspot for the semi-aquatic, and scansorial strategies, whereas the large strategy has pan-tropical hotspots, especially in both the Amazon Basin and Northern Australia, but also in Africa, SE Asia and Mexico.
Surprisingly, we found that functional diversity peaks in areas with medium species richness and slowly decreases toward the speciose areas. This unexpected richness-functional diversity unimodal association is also revealed within the scansorial, large, and semi-aquatic strategies. The richness patterns of terrestrial, nocturnal, herbivorous, and fossorial strategies increase with species richness, but globally functional richness peaks in areas with medium species richness.
Thus increases in richness do not necessarily stem from increased functional diversity. Species diversification within specific strategies often dominates richness patterns.  Our findings support the contention that it is important to consider different functional and ecological subgroups when studying richness patterns.

Author: Shai Meiri
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The Hot Eurasian nightlife - How do different environmental forces affect nocturnality in lizards?

10/10/2017

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In a recent publication in Global Ecology and Biogeography we explored the prevalence of nocturnality amongst Eurasian lizard species and tried to understand what drives these patterns.
Most animals – at least those that live above ground – are active either during the day or during the night. Being active at either time of day carries with it unique benefits and challenges, and thus particular adaptations. Because of this being nocturnal or diurnal is a trait that is pretty rigid amongst closely related species.
Lizards as a group are thought to be ancestrally diurnal. Most of them remain so to this day. Furthermore, they are ectotherms and are predominantly small bodied tetrapods and could thus be particularly affected by the climatic differences between day and night. For this work we collected distribution range and activity time data for all 1,113 lizard species found throughout mainland Eurasia. We then looked at links between richness patterns of lizards with either temperature or productivity.

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Cyrtodactylus trilatofasciatus (Photo: Lee Grismer)
We found that nocturnal lizards have the highest species richness in the tropics and in deserts, and their richness decreases when they get closer to the North Pole. Nocturnal lizards are precluded altogether from the coldest regions inhabited by lizards – in high mountains and the highest latitudes.
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Stenodactylus sthenodactylus (Photo Uri Roll)
Ambient temperature has a strong influence on richness patterns of both diurnal and nocturnal lizards, where species numbers increase with an increase in temperature. Productivity was found to be more tightly related to the proportion of nocturnal species – again in a positive relationship.

We think that our results point towards the fact that low temperatures are a limiting factor for lizard activity period. It is possible that the year-round warm nights of tropic regions enabled lizards to move towards nocturnal activity. In hot deserts, perhaps the combination of hot days and aridity make diurnal activity less attractive, whereas nocturnal activity can provide shelter from these extreme conditions
Author: Enav Vidan
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Stenodactylus doriae (Photo Uri Roll)
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Patterns of species richness, endemism and environmental gradients of African reptiles

28/7/2016

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In our recent publication in the Journal of Biogeography, we assembled a comprehensive distribution map of all reptiles in Africa in order to quantify their geographical overlap with the other vertebrate groups, and to assess the environmental correlates underlying these patterns.
The latitudinal gradient of increasing biological diversity towards the equator is one of the best recognized patterns in biogeography, and has been acknowledged for some time. The naturalist, Alexander von Humboldt wrote of his travels over 200 hundred years ago, that as we approach the tropics, "the greater the variety of structure, form, colour, youth and vigor of organic life." A number of well-known hypotheses explaining this pervasive pattern of the increasing number of different species towards the equator have since proliferated. These include elevated ambient energy and precipitation, the number of different habitats or niches, higher plant productivity, and many more.
Until now reptile diversity gradients have remained largely unmapped and the least studied of the terrestrial vertebrates, especially in Africa. This is an important distinction because reptiles are an extremely diverse class of terrestrial vertebrates (over 10,000 species and counting), and as ectotherms, which often thrive in arid regions, their diversity patterns are thought to differ from the classic latitudinal gradient of the other land vertebrates (amphibians, birds, and mammals). In addition, the distinct reptile lineages - amphisbaenians, crocodiles, lizards, snakes, and turtles are likely to respond differently to environmental variables.

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Vipera palaestinae (photo: Uri Roll)
To create our geographic distribution map of reptiles in Africa, we obtained data from a variety of field-guides and atlases, museum databases, the primary literature, IUCN assessments, and maps based on expert knowledge of reptile species and the habitats they occupy. A challenging aspect of the project was to ensure that our maps remained current with respect to new species discoveries and taxonomic name changes (which are constantly being revised), and we also had to confirm the validity of type specimen identifications and localities, especially those referenced from obscure sources and archaic museum specimens. We used GIS software to digitize and overlay the maps of each individual African reptile species (1,601 species in total!) one on top of the other, which allowed us to count the number of species present in a given area - which we call “species richness”.
Here is the product of all of that hard work - the first comprehensive richness map of all reptile species in Africa. The colour codes correspond to the number of species from low (blue) to high (red). It shows that the reptile richness map is largely congruent with previously mapped amphibian, bird, and mammal richness showing the classic species latitudinal gradient, including high richness in the arid regions not seen in the other vertebrates. But when you look at the reptile groups distinctly you see that while the overall reptile richness map mostly resembles snakes, lizards in particular are qualitatively very different. Lizard richness hotspots are widely dispersed with high diversity in tropical regions, as well as arid and mountainous areas, where the distribution of the other reptile and non-reptile groups is relatively low.

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When we looked at which environmental predictors best explained these species richness maps we found that net primary productivity (the amount of photosynthetic activity by plants) and precipitation explain most of the variation in reptile and other vertebrates. This explains the clear latitudinal pattern seen in their respective maps, which reflects a strong correlation with plant productivity and rainfall as you move closer to the equator. But again, lizards are unique in that none of these environmental correlates explain their distributions. This is because lizards are well adapted to a wide range of habitats including the tropics as well as the harsh conditions of the desert where plant productivity and rainfall are low. We also showed that individual lizard species on average occupy smaller geographic distributions, reflecting their ability to occupy diverse niches.
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Our findings that the distribution of lizard species in Africa is unique when compared to the other vertebrate groups now confirms a pattern that has been seen elsewhere in previous studies (i.e. Australia) and most recently by our paper on the global distribution of reptiles. This shows the importance of studying the diverse reptile groups distinctly instead of lumping them all together, and will have bearing on large-scale conservation efforts that do not represent all reptile groups.
Author: Amir Lewin
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