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Home , Asterophryinae, Caeciliidae, Cryptobatrachus, Flectonotus, List of amphibians, Myersiella

Hydrobiologia (2008) 595:569–580 DOI 10.1007/s10750-007-9032-2

FRESHWATER DIVERSITY ASSESSMENT

Global diversity of (Amphibia) in freshwater

Miguel Vences Æ Jo¨rn Ko¨hler

Ó Springer Science+Business Media B.V. 2007

Abstract This article present a review of species amphibians is very high, with only six out of 348 numbers, biogeographic patterns and evolutionary aquatic genera occurring in more than one of the major trends of amphibians in freshwater. Although most biogeographic divisions used herein. Global declines amphibians live in freshwater in at least their larval threatening amphibians are known to be triggered by phase, many species have evolved different degrees of an emerging infectious fungal disease and possibly by independence from water including direct terrestrial climate change, emphasizing the need of concerted development and viviparity. Of a total of 5,828 conservation efforts, and of more research, focused on species considered here, 4,117 are aquatic both their terrestrial and aquatic stages. in that they live in the water during at least one life- history stage, and a further 177 species are water- Keywords Amphibia Á Anura Á Urodela Á dependent. These numbers are tentative and provide a Á Species diversity Á Evolutionary conservative estimate, because (1) the biology of many trends Á Aquatic species Á Biogeography Á Threats species is unknown, (2) more direct-developing spe- cies e.g. in the , probably depend directly on moisture near water bodies and (3) the Introduction accelerating rate of species discoveries and descrip- tions in amphibians indicates the existence of many Amphibians are a textbook example of organisms more, yet undescribed species, most of which are living at the interface between terrestrial and aquatic likely to have aquatic larvae. Regional endemism in habitats. They fulfil this role both in an ecological context, with typically a strictly aquatic larval and Guest editors: E. V. Balian, C. Le´veˆque, H. Segers & K. Martens largely terrestrial adult phase, and in an evolutionary Freshwater Animal Diversity Assessment context, representing the intermediate bauplan level between aquatic and fully terrestrial M. Vences (&) (‘‘fishes’’ vs. ). Most amphibians are strictly Division of Evolutionary Biology, Zoological Institute, dependent from water for their larval development, Technical University of Braunschweig, Spielmannstr. 8, Braunschweig 38106, Germany and water for this group of is synonym to e-mail: [email protected] freshwater. Although a few amphibians are able to tolerate high-salinity levels (Balinsky, 1981), there J. Ko¨hler are no marine representatives of this class. Department of Zoology, Hessisches Landesmuseum Darmstadt, Friedensplatz 1, Darmstadt 64283, Germany Although existence of an aquatic larval phase e-mail: [email protected] is probably the ancestral condition for recent 123 570 Hydrobiologia (2008) 595:569–580 amphibians, there are only few amphibian taxa with The (aquatic) larvae of and also fully aquatic adult phases. In contrast, multiple are morphologically largely similar to their adults, evolutionary trends towards more terrestrial repro- except for the presence of external gills which usually duction have led to a plethora of reproductive modes are reduced in the adults. In contrasts, the larval stage (Duellman & Trueb, 1986) which make it difficult, in of , the tadpole, is a larval phase radically some instances, to decide if and to what degree a different from the adults (Altig & McDiarmid, 1999). particular species is indeed strictly dependent on Especially the oral and digestive system of tadpoles is freshwater. composed of numerous features which are not Recent amphibians are often named . homologous to the corresponding structures in the They are divided in three orders: frogs (Anura), adult, such as a horny beak, oral papillae and salamanders (Urodela), and caecilians (Gymnophi- keratinous labial teeth, mainly due to the fact that ona). Dubois (2004) recommended abandoning sev- typically tadpoles are omnivorous suspension feeders, eral other higher taxa names based on arguments of ingesting a high degree of vegetable matter, while nomenclatural priority. Although these priority rules adult frogs are strictly carnivorous (with only a single do not strictly apply to names above the family level, known exception, truncata, a species that we here follow Dubois (2004) in not using the names also eats ). Apoda (for caecilians), (for salamanders), Several excellent resources on amphibians were Salientia (for Recent frogs), and available over the world wide web at the time of and (for basal and modern frogs). preparation of the present article. The Amphibian However, we decided to here continue using Liss- Species of the World database (Frost, 2004), hosted amphibia for the clade containing all three recent by the American Museum of Natural History, con- amphibian orders, and we use ‘‘Archaeobatrachia’’ tinues previous efforts (Frost, 1985; Duellman, 1993) and ‘‘Neobatrachia’’ in quotation marks since these to document from a taxonomic point of view all established terms make discussion of anuran rela- amphibian taxa. Amphibiaweb (2005, www.amphib- tionships easier. iaweb.org), hosted by the University of California at Due to the large diversity of extinct Paleozoic Berkeley, provides a full species list of amphibians, amphibians, the phylogenetic relationships of lissam- too, but aims at providing also additional information phibians relative to amniotes has in the past been such as distribution, photographs, and biological data. questioned. Current evidence converges on their The Global Amphibian Assessment (www.globalam- monophyly, based on morphological characters such phibians.org) has compiled, during 2002–2004, the as, for instance, their pedicellate teeth, special visual expertise of regional and taxonomic experts world- cells (green rods) in the retina, or the ear structure wide and provides an estimate of threat status (Duellman & Trueb, 1986), and on molecular char- (according to IUCN criteria) and distribution for all acters (e.g. Meyer & Zardoya, 2003; San Mauro amphibian species. et al., 2005). The paucity of fossils, especially from In this article, we summarize species diversity and the Mesozoic, makes it difficult to trace the early distribution, and zoogeography, of extant amphibians, evolution of lissamphibians, but they appear to be a based on a species list and distributional information very old group according to molecular clocks which compiled from these three online data sources as date the separation among the three orders back into accessed in December 2005. Furthermore, we cate- Paleozoic times before Pangaean break-up (San gorize all amphibian species according to their water Mauro et al., 2005; Roelants & Bossuyt, 2005). dependence on a regional and taxonomical level. For Furthermore, deep divergences are also typical for we generally follow Frost et al. (2006). In amphibians at the species level. As already noted by the following sections, we use the definitions of the Wilson et al. (1974), amphibian species have much freshwater diversity assessment project in defining (1) larger molecular divergences (and, consequently, aquatic species as those with at least part of their life ages) than other vertebrates e.g. mammals and birds, cycle in or on the water, (2) water dependent species and also the large divergences among populations as those which do not live directly in the water but considered to be conspecific are typical for amphib- closely depend on it e.g. for habitat or food, (3) water ians (e.g. Vences et al., 2005a, b). related species as aquatic plus water dependent 123 Hydrobiologia (2008) 595:569–580 571 species, and (4) nor water related species as those more difficult to decide which of the non-aquatic which are neither aquatic nor water dependent. species may be water dependent, i.e. with close/ specific dependence on aquatic habitats (see Figs. 1 and 2). In our categorization, all amphibians charac- Species diversity terized by direct development, viviparity with terres- trial birth, or tadpole development in terrestrial jelly A striking aspect of amphibian taxonomy is the or foam nests are considered to be non-aquatic, while increasing rate of new species discoveries (Glaw & species with tadpoles in water-filled leaf axils of Ko¨hler, 1998;Ko¨hler et al., 2005). As of December plants or tree holes were included in the aquatic 2005, a total of 5,828 amphibian species (aquatic+ category (Figs. 2 and 3). To be able to categorize all non-aquatic) were known, but still at the end of 1992, species, we have here assumed that species share the there were only 4,533 species (Duellman, 1993). The reproductive mode of their closest relatives (usually absolute number of newly described amphibian spe- congeneric taxa). Although certainly not fully pre- cies per decade (not only the cumulative number of cise, this estimate should be a relatively reliable valid and described species) has been steadily approximation to the real situation. In our analysis, increasing since the decade of the 1960s, with species were categorized as ‘‘unknown’’ with respect especially steep increases since the 1990s (Glaw & to their dependence from freshwater only when no Ko¨hler, 1998;Ko¨hler et al., 2005). The new species data at all were available to us concerning the life are in part known populations of described species history of the particular genera. This concerns a small that are found to be genetically or bioacoustically portion of 67 amphibian species only (Fig. 2). distinct, and hence recognized as different species. Several of the non-aquatic species are certainly However, the largest proportion of new species are water dependent. For instance, the South African genuine new discoveries, as exemplified by the recent pyxicephalids of the genera Arthroleptella and spectacular findings of a new lineage, and Anhydrophryne have direct development but usually species in India, (Biju & Bossuyt, live in dense, mossy vegetation around springs and 2003; considered to be part of the family cannot colonize other habitats. Many plethodontid by Frost et al, 2006), and of a new genus and species salamanders have direct development and do not live of plethodontid , Karsenia, in Korea, being in the water, but are predominantly found along the first Asian representative of this family (Min et al., streams because they rely on the humid substrate 2005). This taxonomic progress has been made nourished by the water. These species were placed in possible by the combination of increased field explo- category ‘water dependent’. Nevertheless, there cer- ration in tropical regions, together with the application tainly are species which are fully independent from of molecular and bioacoustic techniques becoming water, such as the desert-dwelling species of Brev- routine. A case study in Madagascar indicated that iceps which occur far from any water body and newly discovered species since 1990 are genetically depend on air humidity only. Several direct-develop- not less distinct from already described species than ing frogs of the genera Craugastor, Euhyas and species discovered in the research periods before, and Eleutherodactylus live in bromeliads, and probably that the increase in new species is not a sign of depend on the moisture provided by water-filled taxonomic inflation due to exaggerated splitting phytotelmes. However, since the life habits of very approaches (Ko¨hler et al., 2005). few species in this species-rich genera were studied, Of the total of 5,828 amphibian species considered we here found it premature to decide which and how here, 4,117 are aquatic in that they live in the water many species are non-aquatic but water dependent. during at least one life-history stage, and a further As we did in the genera Craugastor, Euhyas and 177 species are water dependent. By the end of 2005, Eleutherodactylus, we considered all non-aquatic there were a total of 168 species of caecilians, 514 species where natural history observations are sparse salamanders and 5,146 frogs. While it is relatively also as non-water dependent, which is probably true straightforward to decide which of these are, under for the majority of these species. However, it is the definitions used here, real aquatics (i.e. with at implicit in this procedure that the numbers provided least part of the life cycle in or on the water), it is in Tables 1 and 2 will be slight underestimates. 123 572 Hydrobiologia (2008) 595:569–580

Fig. 1 Map showing species and genus diversity of water related amphibian species by major zoogeographic divisions. PA, Palearctic; NA, Nearctic; NT, Neotropical; AT, Afrotropical; OL, Oriental; AU, Australasian; PAC, Pacific Oceanic Islands; , Antarctic. Numbers include aquatic amphibian species (with at least one aquatic life-history stage) plus those that are water dependent (e.g. some direct-developing species)

caecilians, species of the family Caeciliidae are reported to have aquatic adults with viviparous reproduction. However, ecological studies suggest that at least some species may not be strictly aquatic but actually display a semi-aquatic behaviour with resting periods out of water and foraging in aquatic habitat (Moodie, 1978). Among salamanders, fully aquatic families are the Cryptobranchidae, Amphi- umidae, , and , and aquatic adults also occur in the genus Ambystoma. In many of these species, for example in the well-known Axolotl, Ambystoma mexicanum (), the aqua- tic adults are paedomorphic (neotenic), and retain larval features such as external gills and a fully Fig. 2 Percentages (rounded) of amphibian species in catego- functional lateral-line system. ries aquatic, water dependent, not water related and unknown according to the definitions used herein. Together, the The most extreme modifications of reproductive categories aquatic and water dependent are summed up as modes are those that completely eliminate the free- ‘Total’ in Tables 1 and 2 living larval phase: direct development, and some- times viviparity. Viviparous and ovoviviparous Historical processes: evolutionary trends away amphibians are relative rare, but caecilians are an from and towards water exception where about 75% of the known species are considered to have a viviparous mode of reproduction As outlined above, fully aquatic adult amphibians are (Himstedt 1996). Members of the Neotropical genus rare. Among anurans, only representatives of the Typhlonectes and of the Afrotropical genus Scolec- family qualify as such plus very few species omorphus are exclusively viviparous, and viviparity of other families, while among salamanders and also occurs in some other genera of the family caecilians, an aquatic life history is more common. In Caeciliidae. In salamanders, viviparous species are 123 Hydrobiologia (2008) 595:569–580 573

viviparity is known only in the two African bufonid genera Nectophrynoides and Nimbaphrynoides, and in the brachycephalid Eleutherodactylus jasperi (see Wake, 1977; 1989). All viviparous frogs bear fully metamorphosed young and therefore have no aquatic larval stage. Viviparous salamanders can bear meta- morphosed young or (aquatic) larvae. Caecilians of the genus Typhlonectes are viviparous with aquatic larvae, whereas other viviparous caecilians have no larval stage. In pipid frogs of the genus Pipa, the eggs are embedded in the dorsum of the (aquatic) female and thus indirectly undergo development in an aquatic environment; in all other cases, direct-devel- oping amphibians lay terrestrial eggs. Direct development has evolved independently in many amphibian lineages: in salamanders once in the family , which contains almost exclu- sively direct developers; in caecilians, in the family Caeciliidae; and among anurans in many of the major lineages: (1) in the basal Leiopelmatidae, genus from New Zealand; (2) in sooglossids (genus Sooglossus); (3) in some species of the genus Pipa (Pipidae); (4) in some genera of myobatrachids; (5) in brachycephalids; (6) in (genus ); (7) in Cryptobatrachidae (genera Cryptobatrachus, ); (8) in Amphi- gnathodontidae (genera Flectonotus, Gastrotheca); (9) in several genera of bufonids (e.g. Oreophrynella, Osornophryne, Rhamphophryne); (10) in the genus Platymantis (); (11) in Pyxicepha- lidae (Arthroleptella and related genera); (12) in at least one dicroglossid species (Limnonectes hasche- anus); (13) in several species of one genus of mantellids (Gephyromantis; see Glaw & Vences, 2006); (14) in at least one genus of rhacophorids (Philautus); (15) in brevicipitids (Breviceps and related genera); (16) in Australasian microhylids (subfamily Asterophryinae); (17) in few Neotropical microhylids (Myersiella, Synapturanus); (18) in sev- eral arthroleptids (genera Arthroleptis, Schoutedenel- la). Hence, altogether there are at least 18 independent evolutionary events towards direct development in Fig. 3 Percentages (rounded) of frog (A), salamander (B) and anurans, while this reproductive mode has evolved (C) species in categories aquatic, water dependent, not water related and unknown. Together, the categories only once in salamanders and probably twice in aquatic and water dependent are summed up as ‘Total’ in caecilians. It needs to be emphasized that these are Tables 1 and 2 minimum estimates, and especially in frogs it is likely that more complete phylogenetic data will provide found exclusively in the (genera evidence that direct development evolved even more Salamandra and Lyciasalamandra). Among frogs, commonly in parallel. 123 574 Hydrobiologia (2008) 595:569–580

Interestingly, some of the direct-developing amphibian lineages are characterized by a very high species richness. The Brachycephalidae contain approximately 800 direct-developing species, and among salamanders, the largely direct-developing Plethodontidae encompass by far the largest number of species (349 out of a total of 514 salamander ions). PA : Palearctic; NA species). This may be seen as indication that water- independence is a particularly successful strategy for amphibians. It could also be a by-product of a putative higher fragmentation into isolated demes in direct developers, which may lead to an increased rate of species formation (Dubois, 2005). Studies that apply comparative methods to test against null models, and population genetic studies of direct developers are necessary to clarify this question. Remarkably, recent phylogenetic evidence indi- cates that in a number of groups of predominantly direct development, some lineages have reversed their reproductive mode and re-acquired an aquatic larval stage. This appears to be the case in pleth- odontid salamanders, Desmognathus, as well as in some amphignathodontid frogs, Gastrotheca, and possibly in mantellid frogs as well (Duellman & Hillis, 1987; Vences & Glaw, 2001; Chippindale et al., 2004). These reversed trends emphasize the selective advantage, under at least some evolutionary conditions, of biphasic aquatic-terrestrial life cycles, and the importance of freshwaters for amphibian diversity.

Distribution and endemicity

Amphibians are in general considered to be poor dispersers, and the strong phylogeographic structure encountered in many amphibian species (e.g. Avise, 2000) appears to support this view. Due to their limited osmotic tolerance, overseas dispersal was long neglected as dispersal mechanism for amphib- ians, and their zoogeographic patterns explained largely by vicariance and dispersal over land con- nections (e.g. Duellman & Trueb, 1986). Evidence

PA NA NT ATfrom molecular OL clocks AU and the discovery PAC of ANT endemic World amphibians on oceanic islands, such as Mayotte on the Comoros, provide strong support that amphibians Numbers of water related amphibian species by order are able to colonize landmasses over the sea (e.g. Hedges et al., 1992; Vences et al., 2003; 2004).This : Nearctic; NT : Neotropical; AT : Afrotropical ; OL : Oriental; AU : Australasian; PAC : Pacific Oceanic Islands, ANT: Antarctic Table 1 OrderAnuraUrodelaGymnophiona FWTotal WDpt 68 0 92‘FW’ FW refers to aquatic plus water dependent WDpt species, WDpt to 0 water 0 dependent only 0 (of 160 a total of FW 5828 89 amphibian species 114 considered; see 0 text WDpt for definit 0 FW 48 0 203 WDpt 0 1,661concerns 14 FW 48 23 21 WDpt 1,698 0 816 FW frogs, 0 WDpt 21 0 73 12 FW 828 but 1,001 WDpt may 0 FW 73 0 WDpt 1,062 0 also 17 44 301 FW apply 0 WDpt 0 35 0 301 to 0 0salamanders 0 35 0 0 0 0 0 0 0 0 0 0 0 0 3,978 0 0 0 129 4,294 0 0 177 237 79 48 0 123 Hydrobiologia (2008) 595:569–580 575

Table 2 Numbers of amphibian genera including aquatic and water dependent species according to the definitions used herein by order Order PA NA NT AT OL AU PAC ANT World

Anura 8 9 119 85 64 20 0 0 294 Urodela 18 18 1 0 4 0 0 0 40 Gymnophiona 0 0 7 4 3 0 0 0 14 Total 26 27 127 89 71 20 0 0 348 For the subfamily , the classicatory scheme of Faivovich et al. (2005) is followed. However, all other numbers in genera have not been updated and refer to a taxonomy prior to the publication of Frost et al. (2006). Therefore, some genera were supposed to occur in more than one biogeographic region and thus the sums of all regional numbers are higher than the total numbers. PA : Palearctic; NA : Nearctic; NT : Neotropical; AT : Afrotropical; OL : Oriental; AU : Australasian; PAC : Pacific Oceanic Islands, ANT: Antarctic and even caecilians, as indicated by the presence of & Bossuyt, 2005), in accordance with morphological an endemic caecilian species, Schistometopum tho- hypotheses (e.g. Duellman & Trueb, 1986). Further- mense, on the fully volcanic Sa˜oTome´ island in the more, also the distributional patterns observed leave Gulf of Guinea (Measey et al., 2007). Nevertheless, it room for the assumption that not only causes of remains true that amphibian distributions have cer- vicariance biogeography, but also of ecological tainly largely been shaped by vicariance, as shown by requirements have shaped the distribution of the relationships of relict forms such as the Seychellean three amphibian orders. sooglossid frogs and the Indian Nasikabatrachus Salamanders are almost exclusively distributed on (Biju & Bossuyt, 2003). previous Laurasian landmasses to which 9 of the 10 At the deep phylogenetic levels, there are clear salamander families are restricted, if the presence of a distributional trends of salamanders and basal frogs few representatives of salamandrids (Salamandra and having their centres of diversity in the Holarctis and Pleurodeles) in northern Africa is disregarded. This caecilians and modern frogs in the tropics. Since pattern is obscured by the fact that one large radiation some phylogenetic reconstructions placed caecilians of one family, the Plethodontidae, has colonized the as sister group of salamanders, and both basal and Neotropics and attains a high species diversity in modern frogs (‘‘archaeobatrachians’’ and ‘‘neobatra- Mexico and Central America. Indeed, 252 salaman- chians’’) as monophyletic groups, the distributional der species occur in the Neotropics as defined here, patterns of these lineages were interpreted by some more than in any other biogeographic region. How- phylogeneticists as indicative of vicariance during the ever, only few species of two genera, Bolitoglossa break-up of Pangaea into the Laurasia and Gondwana and Oedipina, have penetrated further into South supercontinents, with caecilians and ‘‘neobatra- America, leaving no doubts that northern America chians’’ evolving and diversifying on Gondwana, was the initial centre of diversification of this family. and ‘‘archaeobatrachians’’ and salamanders diversi- Almost all plethodontids are characterized by direct fying on Laurasia (Feller & Hedges, 1998). development, and are therefore less relevant in the Recent phylogenetic evidence, however, does not present survey of freshwater diversity, most species support this hypothesis. Evidence from complete not being included in Table 1. Salamanders have mitochondrial sequences and nuclear genes indicates almost not penetrated into tropical areas of Asia, that frogs and salamanders, not salamanders and although there are salamandrids occurring as far to caecilians, are sister groups (Meyer & Zardoya, 2003; the south as Laos and Vietnam. San Mauro et al., 2005; Frost et al., 2006). In Caecilians have a distribution fully restricted to the addition, phylogenetic reconstructions based on dif- tropics. They are found in the Neotropical, Afrotrop- ferent nuclear genes are concordant in establishing ical and Oriental regions. Interestingly, although paraphyly of basal frogs (‘‘archaeobatrachians’’) endemic caecilians are present on the Seychelles, relative to the monophyletic ‘‘neobatrachians’’ they are absent from Madagascar. Caecilians do not (Hoegg et al., 2004; San Mauro et al., 2005; Roelants occur in southernmost South America, or in southern 123 576 Hydrobiologia (2008) 595:569–580

Africa, indicating that the limiting factor for their groups together. Monophyly of these ‘‘modern frogs’’ distribution is indeed the presence of tropical-humid is well established by molecular and morphological environments. Apart from climate which obviously characters (Duellman & Trueb, 1986; Hoegg et al., triggers the current distribution of caecilians, it has 2004; Roelants & Bossuyt, 2005; San Mauro et al., been assumed that radiation in caecilians largely took 2005). Their largest diversity belongs into two place before Gondwana split into sub-continents. subgroups, the hyloids, with a centre of diversity in Some families like the South American Rhinatremat- the Neotropics, and the ranoids, with a centre of idae and the Asian are supposed to diversity in Africa and Asia. represent relict distributions of formerly widespread Ranoids, according to the scheme of Frost et al. Gondwanan ancestors (Duellman & Trueb, 1986), (2006), include families restricted to Africa and/or whereas some Neotropical members of the Caecilii- Madagascar, such as the , Hemisotidae, dae (e.g. Typhlonectes) possibly are the product of , , Phrynobatrachidae, Pty- subsequent radiations on the already isolated South chadenidae and ; two mainly Asian American continent (Himstedt, 1996). families with few African representatives, the Rhac- Basal frog lineages (‘‘archaeobatrachians’’, de- ophoridae and ; two South Asian fined as a paraphyletic group of all extant frogs not families, the and Microxalidae; belonging to the modern frogs or ‘‘neobatrachians’’) one South-East Asian family, the Ceratobatrachidae; are mainly distributed in the Holarctis, with four one family present in Africa and Asia, and that notable exceptions, however. (1) Pipids, the only succeeded to colonize also North and South America, frogs which are fully aquatic also in their adult stage, the ; and the species-rich Ranidae that have a clearly Gondwanan distribution, with genera colonized Europe as well as North and South in Africa (Xenopus, Silurana, Pseudhymenochirus America. The Pedropeditae sensu Frost et al. (2006) and Hymenochirus; 23 species) and in South America contain African and South Asian species, although (Pipa; 7 species). (2) Leiopelmatidae: the genus these relationships require further corroboration. Leiopelma (4 species) occurs in New Zealand, Hyloids include several families restricted to the although its closest relative, Ascaphus, is restricted Neotropics, such as the , to the Nearctis. (3) The discoglossid genus Barbour- Brachycephalidae, , Centrolenidae, ula occurs on Borneo and the Philippines, whereas its Cryptobatrachidae, , Dendrobatidae, closest relatives, the genus Bombina, has a Palearctic Hemiphractidae, , Thoropidae; one distribution. And (4) the Megophryidae, with 72 family, the Bufonidae, common in the Neotropis with species by far the largest ‘‘archaeobatrachian’’ fam- also many representatives in the Palearctic, Nearctic, ily, has radiated in the Oriental region and is common Oriental, and Afrotropical regions, including genera in tropical environments. Based on a robust molec- endemic to the main biogeographical regions; and ular phylogeny and molecular clock dating, Roelants one family, the , with many species in the & Bossuyt (2005) found evidence for three major Neotropis, which has representatives also in the cladogenetic events between a Laurasia- and a Nearctic, Palearctic and Australian region. Gondwana-associated lineage, represented by Asca- Besides hyloids and ranoids, a number of further phus and Leiopelma, Rhinophrynidae and Pipidae and ‘‘neobatrachian’’ families exist. Into this assemblage Pelobatoidea and ‘‘Neobatrachia’’, respectively, all belong the sooglossids from the Seychelles and these splits being very close to the onset of Pangaean southern India, as well as heleophrynids from South break-up at 180 mya. Although this pattern substan- Africa, limnodynastids and myobatrachids from tiates a high-biogeographic relevance of ‘‘archaeoba- Australia and New Guinea and the Batrachophryni- trachians’’, they altogether make up only a negligible dae from South America. part of overall frog diversity, with a total of 191 of While providing a general zoogeographic picture the total of 5,146 frog species (including non-water for amphibians or discussing the possible prevalence related taxa). of vicariance vs. dispersal hypotheses, is clearly ‘‘Neobatrachians’’, with 4,955 species, do not only beyond the scope of this article, a number of general form the most speciose anuran subgroup, but also patterns can still be discerned from the distributions include by far more species than all other amphibian outlined above: 123 Hydrobiologia (2008) 595:569–580 577

(1) At a very fundamental level, the influence of manders and ranid frogs, and the colonization of vicariance is very clearly visible in a number of the Palearctis by hylid frogs, almost certainly amphibian distributions. Although salamanders represent such instances. At the interface and caecilians are certainly limited in their between dispersal and vicariance, the hylid distribution by adaptations to temperate vs. subfamilies (Australian) and tropical environments, their general patterns of Phyllomedusinae (Neotropical) are sister groups geographic occurrence and the restriction of (Hoegg et al., 2004; Frost et al., 2006), and salamanders to temperate regions of the north- probably are witnesses of a vaster distribution of ern hemisphere make it likely that the basal these tree frogs while South America and diversification of salamanders occurred on Australia were connected over Antarctica in Laurasia and that of caecilians on Gondwana the Early Cenozoic. During this time, probably, (Feller & Hedges, 1998). ‘‘Archaeobatrachians’’ the ancestor of these frogs dispersed from South are separated in a number of lineages of America to Australia, and the two groups alternatingly Laurasian or Gondwanian distri- evolved in vicariance after the continental bution (Roelants & Bossuyt, 2005). The distri- connections were severed. bution of basal neobatrachians in the southern (3) A third factor that should not be underestimated hemisphere indicates that they initially had a is (natural) extinction. There is impressive Gondwanan distribution. And the diversity evidence in current amphibian distributions for centres of hyloid vs. ranoid neobatrachian frogs formerly larger distribution areas of groups of in the New World vs. the Old World (and here, today relictual occurrence. Among the examples especially Africa) are likely to correspond to the are the relationships between Ascaphus and separation of South America and Africa, which Leiopelma (Leiopelmatidae), the most basal of also roughly agrees with molecular clock the extant anurans, and with two and four calculations (e.g. San Mauro et al., 2005; species restricted to the Western North Amer- Roelants & Bossuyt, 2005). ica, and to New Zealand respectively. Pleth- (2) The initial pattern originated by vicariance has odontid salamanders are today most diverse in been modified extensively by dispersal. The the Nearctis and Neotropis, but one genus, occurrence of some endemic amphibians on Speleomantes, is known from Italy and France. oceanic islands is a clear evidence for the The very recent discovery of the first Asian possibility of overseas dispersal also in this plethodontid Karsenia by Min et al. (2005) group. The phylogenetic split of several lin- clearly demonstrates that this group had a wider eages like the reed frogs, Hyperoliidae, are so distribution in Asia and Europe before, and young according to molecular clocks that their probably went extinct over most of its Palearctic occurrence in Madagascar and on the Seychelles distribution area. Again, also the relictual dis- can only be seen in colonization by ancestors tribution of the basal ‘‘neobatrachian’’ frogs in rafting on flotsam over the sea (Vences et al., southern South America, Australia, South Afri- 2003). The few genera occurring in more than ca, the Seychelles and India probably witnesses one biogeographic region and continent provide a previous, much wider Gondwanian distribu- further evidence for the possibility and potential tion. Probably, and especially in frogs, succes- speed of amphibian dispersal. The genus Hop- sive waves of radiation of more modern groups lobatrachus has a number of species in Asia, have largely replaced the more basal groups and has one Afrotropical species that colonized, which survived, if at all, as species-poor relicts out of Asia, vast areas of the African savannas in very restricted and fragmented distribution in short time spans, as to judge from the low areas. molecular differentiation among Asian and Due to their relatively limited dispersal ability, by African Hoplobatrachus species (Kosuch far most amphibian genera, and almost all amphibian et al., 2001). Similar examples can be found in species, are endemic to single continents or biogeo- other genera and families as well. The coloni- graphic units. These units largely correspond to the zation of South America by plethodontid sala- 123 578 Hydrobiologia (2008) 595:569–580 biogeographic regions used here. Some additional ate threat to most amphibians in a threatened IUCN subdivisions are obvious (of course not considering category is habitat destruction, and for some species introductions): In the Afrotropical region, all species overexploitation (as pets or food) constitutes an and all genera but one occurring in Madagascar are imminent danger as well. endemic to the island (with two genera of mantellid The Global Amphibian Assessment (Stuart et al., frogs also having one species each endemic to the 2004) classified 1856 amphibian species (32.5%) into Comoro island of Mayotte); and all genera and one of the IUCN threat categories (Vulnerable, species of Seychellean caecilians and frogs are Endangered or Critically Endangered), many more endemic to the archipelago. Sub-Saharan Africa than in other groups such as mammals (23%) or birds shares no amphibian species with Asia or Europe, (12%). About 43% of all species were recorded to and the species-level of endemism of Australia is experience some sort of population decline. A total of above 90%. Further islands with a degree of ende- 32 amphibian species have become extinct, and 122 mism of 100% at the species level are Jamaica, Sa˜o species were considered to be ‘‘possibly extinct’’, Tome´ and Principe, New Zealand, Fiji and Palau with no recent sightings. (percentages based on analyses including non-water Most alarmingly, so-called enigmatic declines related amphibian species; see http://www.globalam- have also been reported from unaltered and largely phibians.org/patterns.htm for a more detailed analysis undisturbed habitats, especially in South America and based on the data from the Global Amphibian Australia, but also in North America and Europe Assessment). (Blaustein et al., 1994). Furthermore, it has been Most of the few genera with distributions extend- shown that the absence of aquatic larvae in declining ing over more than one of the main zoogeographic anuran populations may significantly alter freshwater regions, all of them frogs, were classical ‘‘dump bin’’ ecosystems (Ranvestel et al. 2004). Most likely, genera which were recently split into various genera emerging infectious diseases, especially chytridiomy- after comprehensive revisions (Faivovich et al., 2005; cosis, play a key role in these declines which in many Frost et al., 2006). For example, the formerly 340 cases apparently have led to full extinctions already species of Hyla with representatives in the Neotropis, (Daszak et al., 2003). The chytrid fungus Batracho- Orientalis, Nearctis and Palearctis have recently been chytrium dendrobatidis especially affects species that taxonomically revised and were split into 15 genera, are ecologically predisposed in that their natural with the genus Hyla now being restricted to few history (high-altitude occurrence, stream breeding) species in the Nearctic and Palearctic regions coincides with the preferences of the pathogen, and if (Faivovich et al. 2005). In addition, only the frog combined with low fecundity and habitat specializa- genera Hoplobatrachus (Orientalis with four and tion, a species can quickly be driven to extinction Afrotropis with one species) and Ptychadena (one (Daszak et al., 2003), and this process may be species in Palaearctis as defined herein, all others in furthered by climatic change (Pounds et al., 2006). Afrotropis) have a distribution across biogeographic Interestingly, despite high degrees of chytrid infec- regions, and the salamander genus Ambystoma has 15 tion in the wild, no African frogs have yet been Nearctic and 14 Neotropical representatives; how- reported to have enigmatically declined, which led ever, the Neotropical species are restricted to Mexico Weldon et al. (2004) to hypothesize that the disease and the genus did not further disperse into Central or may have originated in Africa and spread to other South America. continents by exported clawed frogs, Xenopus,as carriers. The important role of chytridiomycosis in amphib- Human related issues: global amphibian declines ian declines has been asserted, and obvious measures include the control of amphibian introductions into More new amphibian species are being discovered unaffected areas as well as the disinfection of fishing every year than ever, but at the same time, amphib- gear and similar equipment by limnologists working ians are paradoxically declining at a very fast rate on different continents. However, the influence of (Hanken, 1999). Multi-causal declines have been other agents such as pesticides or increased UV recorded worldwide. The most obvious and immedi- radiation should not be disregarded, and multi-causal 123 Hydrobiologia (2008) 595:569–580 579 hypotheses may well be most powerful to explain Duellman, W. E. & D. M. Hillis, 1987. Marsupial frogs (An- declines in some cases. 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