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Home , Aromobatidae, Blommersia, Buergeria, Caecilian, Dendropsophus ebraccatus, Hyla savignyi

a Frontiers of 2019, 11.4, e44577

Frontiers of Biogeography Review the scientific journal of the International Biogeography Society

Long-distance dispersal in

Luis Fernando Marin da Fonte1,2*, Michael Mayer1 and Stefan Lötters1,2

1 Biogeography Department, Trier University, Trier, Germany; 2 http://www.stefanloetters.de *Correspondence: Luis Fernando Marin da Fonte, Biogeography Department, Trier University, 54286 Trier, Germany. E-mail: [email protected].

Abstract Highlights Although the distribution patterns of major • This is the most complete and up-to-date review of lineages are mainly explained by a Pangean origin with long-distance dispersal (LDD) in amphibians, compiling subsequent vicariant diversification, dispersal events have information from more than 70 articles. exerted a strong influence on present-day distributions. Long-distance dispersal (LDD) involves movements outside • Although amphibians are considered poor to moderate the standard geographic limits and outside the genetic dispersers, we show that they do perform LDD. neighbourhood area of individuals. Although considered ‘rare’, LDD is disproportionately important to amphibian • We propose that 10 km is a reasonable threshold for populations, and communities. To understand the amphibian movements to be considered LDD. role of LDD in shaping current biogeographic patterns in • The longest active LDD movement recovered in our these , we reviewed the cases reported in the bibliographic search was 34 km. literature. A systematic bibliographic search was performed to obtain information on how many studies have dealt • Passive overwater LDD events by means of rafting with LDD in amphibians, which methods they used, which include movements of around 1,000 km across oceans. taxa and distances were involved, and when/where events had apparently occurred. In 41 studies, we recovered at least 90 LDD events (3 active, 87 passive) involving at least 56 extant species and 38 genera. Most events (73) involved the colonization of islands, with rafting being suggested as the most conceivable means of overwater passive dispersal for these . In this review, we show that LDD events have played an important role in shaping current amphibian biogeographic patterns, especially the occurrence of disjunct distributions and the colonization of islands.

Keywords: Anura, Biogeography, , , island colonization, jump dispersal, overwater dispersal, transoceanic movement

Introduction view that changes occur not gradually but rapidly and abruptly (cf. Halstead 1980). Some decades ago, there was a fierce debate in With the rise of the vicariance school (cf. Croizat, biogeography over the most appropriate method for Nelson and Rosen 1974), dispersal was considered by analysing species formation and distributions, i.e., cladistic biogeographers (e.g., Nelson and Platnick 1981) conventional evolutionary vs. as ‘unfalsifiable’ and ‘untestable’ and thus simply not (Stoddart 1981). At that time these two methods scientific. Over the last decades, however, the advance were seen as opposites, and there was open hostility of molecular techniques and the revision of geological between the battle lines (Rosen 1981: 3). Discussions time calibrations have allowed for a refinement of were so intense that the two sides accused each other biogeographic studies. This now enables researchers of political motives for their views. Wallace‑Darwinian to make accurate predictions of divergence dates and dispersalism was regarded as imperialistic and colonialistic, locations of sister lineages, turning dispersal suggestions for it would require colonization, competition and into subjects of refutation (de Queiroz 2005). Despite dominance (cf. Nelson 1978, Rosen 1981: 2). Cladistics the predominance of the vicariance paradigm during were regarded as Marxist, for it would reflect the the final decades of the last century, recent genetic e-ISSN: 1948-6596 https://escholarship.org/uc/fb doi:10.21425/F5FBG44577

© the authors, CC-BY 4.0 license 1 Fonte et al. Long-distance dispersal in amphibians studies based on molecular clock calibration have it is typically arbitrary, its order of magnitude should resurrected the debate, strengthening the importance reasonably reflect the scale of the process in question of long-distance movements, such as across oceans (Nathan 2005). and seas (de Queiroz 2005, 2014). As a rule of thumb, LDD is usually mediated by passive movement (Shigesada and Kawasaki 2002) and Dispersal is therefore also referred to as occasional dispersal (de Dispersal definitions vary greatly and are therefore Queiroz 2014). Yet, passive LDD should not be seen as usually confusing, mainly depending on the organism ‘accidental’ or ‘random’ dispersal because statistical and scale considered. In a broad sense, dispersal can probability can aid in predicting which organisms be defined as movement leading to spatial , are more often transported to given places based on whatever the behaviour or movement mode giving knowledge of natural history, direction of currents rise to it (Ronce 2007, Clobert et al. 2012). Although and winds, etc. (Darlington 1938). dispersal is an individual-based process, its consequences frequently scale up to the level of population properties Movement in amphibians (Jordano 2017). In this sense, rather than being relegated Amphibians are the most extant tetrapods. to a distance measurement, dispersal should be seen Modern amphibians, comprising three orders, are as a process leading to a distributional outcome of the usually small and possess physiological properties (e.g., movement itself (Dingle 1996). their highly permeable skin) that make movements Because dispersal definitions vary so much, it is costly so that they only move when necessary (Wells important to define some concepts that we use in this 2007). Smith and Green (2005) compiled information paper. Normal dispersal is the expected movement from 166 articles on 90 living amphibian species and of organisms within continuous tracts of suitable found that 44% of them actively moved no farther or between patches of suitable habitat that than 400 m, while just 5% were capable of movements are close together (de Queiroz 2014). It is also called greater than 10 km. They also found differences short-distance dispersal or diffusion (Pielou 1979) between orders, with 44% of the anuran and just and its result is the (more or less) steady expansion 6% of the species displaying maximum of the species range. Long-distance dispersal (LDD) active dispersal distances greater than 1 km. Based involves movements outside the standard geographic on an inverse power law, Smith and Green (2005) limits and outside the genetic neighbourhood area of predicted that, for anurans and , at least individuals (Jordano 2017), often involving movement one individual is likely to move distances of 11-13 km across barriers (de Queiroz 2014). We consider jump and 8-9 km, respectively. Considerably less is known dispersal as LDD that is performed in a markedly short about movement patterns in . The maximum period of time followed by successful establishment distance found by a mark‑recapture study was 4.5 m of a population (cf. Pielou 1979). In active dispersal, away from the point of release (Measey et al. 2003), the organism accomplishes (or contributes to) the suggesting that caecilians are exceptionally poor dispersal process through control of its own locomotion, dispersers, but further study is needed to characterize whereas in passive dispersal the movement is largely the dispersal behaviour of this group with any reliability. outside the organism’s immediate control, depending Because amphibians are generally poor to moderate on external forces such as gravity, wind, water, and active dispersers and often philopatric, most species carrier organisms (Mattysen 2012). formation in this group is vicariant, principally dichopatric, that is, resulting from range subdivision Long-distance dispersal (Vences and Wake 2007). In a large-scale historical LDD events are infrequent and scattered, but given biogeographic analysis involving approximately 45% of sufficient time, their occurrence over time becomes extant amphibians, Pyron (2014) found that Pangean increasingly probable (Darlington 1938, Stoddart 1981). origin and subsequent Laurasian and Gondwanan Although considered rare, LDD is disproportionately fragmentation explain a large proportion of patterns important to populations, species, and communities in the distribution of extant species. In line with this, (Nathan 2005, 2006), for it has a strong influence on several other phylogenetic studies found similar patterns gene flow and the structure of gene pools (Jordano (i.e., Roelants and Bossuyt 2005, San Mauro et al. 2017). Besides enabling the maintenance of genetic 2005, Bossuyt et al. 2006, Feng et al. 2017; for more connectivity between disparate populations, LDD examples of vicariant species formation in amphibians, can also lead to the colonization of vacant see Vences and Wake 2007). Nevertheless, and thus range expansions, driving population and dispersal have also exerted a strong influence diversification, including (Jordano 2017). on present-day distributions (Vences and Köhler In general, populations founded as a result of LDD 2008), including normal dispersal (i.e., terrestrial (especially jump dispersal) tend to diverge from range expansion and land-bridge colonization) and the source populations. The founder and source overwater/stepping-stone events (Pyron 2014). populations are genetically isolated from one another In fact, some occurrence patterns, such as the because movement between them is hampered per se presence of amphibians on oceanic islands (i.e., that (de Queiroz 2014). The threshold defined for a dispersal were never connected with continental landmasses), event to be considered long‑distance vs. normal varies can only be explained by overwater jump dispersal according to the of the organisms, and although events. In this regard, it is noteworthy that from

Frontiers of Biogeography 2019, 11.4, e44577 © the authors, CC-BY 4.0 license 2 Fonte et al. Long-distance dispersal in amphibians

Darwin’s time (1859) until recently, it was believed water for up to four days without losing their capacity that amphibians could not traverse long distances for development. Kleyheeg and van Leeuwen (2015) across oceans because of salt intolerance and the studied the potential of regurgitation by birds as means risk of dehydration. Yet, recent reviews have shown of and suggested that, if regurgitation that some degree of salt tolerance exists in more occurs only a few hours after ingestion, it could also amphibian taxa than had previously been assumed facilitate dispersal of less resistant organisms, such as (Hopkins and Brodie 2015). Moreover, certain lineages – in this case – fish eggs. Fahr (1993) and Measey et al. may in fact have dispersed across oceans several (2007) discussed bird carriage as a mechanism by times in their evolutionary history (de Queiroz 2005, which amphibians may have colonized the Gulf of 2014). In amphibians, this paradigm shift has even Guinea islands. Although the authors did not rule out led to the revision of previous hypotheses, such as this possibility, they considered it unlikely. Despite the vicariant origin of eleutherodactyline in the never having been documented, passive dispersal (Hass and Hedges 1991, Hedges 1996) in of amphibians (especially eggs and larvae) by other favour of overwater dispersal from could be possible, although survival of the (Heinicke et al. 2007). amphibians may be unlikely. Study goals Humans Recent reviews (e.g., de Queiroz 2005, 2014) Human-mediated introduction of species in new have proposed that LDD events involving a variety of areas, sometimes even on continents other than the amphibian taxa and geographic regions have indeed species’ origin, can result in non-native established taken place over geologic time. Our purpose here is to populations. Kraus (2009) compiled worldwide test this hypothesis and to determine the frequency information on so-called alien species with regard to of LDD in amphibians. Because these vertebrates are amphibians, reporting more than 1,200 introduction generally poor to moderate active dispersers, they events, involving ca. 180 species in ca. 600 localities. are usually highly structured genetically over short Although we recognize the importance of such LDD geographic distances and retain high-resolution signals events, especially the potential of humans to introduce of historical events that generated current species invasive species and spread diseases, in our paper distributions (Zeisset and Beebee 2008). Moreover, we will not focus on this topic given the already vast they typically show high levels of geographic variability literature on it. in molecular markers (Vences and Wake 2007). For these reasons, they tend to be suitable models Air for the study of different biogeographic hypotheses, Although never proven, there are several published including long‑distance movements such as jump anecdotal reports of ‘rains’ (e.g., McAtee 1917, Elsom dispersal across oceans. To understand the role of 1988), and some scientists have claimed that strong air LDD in shaping current biogeographic patterns in currents and waterspouts can lift and transport these amphibians, we review the cases for these tetrapods animals. For instance, Darlington (1938) speculated that reported in the literature. For an introduction to the amphibians could have reached the Greater Antilles topic, we first present a general descriptive overview islands via dead palm leaves transported by hurricanes. of amphibian passive LDD. Subsequently, based on Nevertheless, such dispersal events of vertebrates are a systematic review of the literature, we provide usually considered unimportant, for the animals should definitions of active and passive LDD in amphibians be carried for short distances, reach unfavourable and discuss the principal cases. environments and often arrive dead (McAtee 1917). Even so, it is important to note that high wind events Overview of passive LDD in amphibians (i.e., cyclones, typhoons, hurricanes) combined with heavy rains might create favourable conditions for the Since LDD events are typically ‘rare’ (Nathan dispersal of floating rafts over large distances across 2005), they are seldom observed (Stoddard 1981). bodies of water (see below). In amphibians, rafting has been suggested as the most conceivable means of overwater jump dispersal Water (e.g., Hedges 1996, Vences et al. 2003, Measey et al. Driftwood, rafts, and floating meadows can be carried 2007). In addition, the less-likely cases of storm and by river and marine currents over large distances, even bird carriage have been discussed by earlier works crossing oceans and arriving at distant continents (Darlington 1938) as well as more recent analyses (Barber et al. 1959). Schuchert (1935), for instance, (e.g., Measey et al. 2007). All these possible routes of reported the occurrence of rafts that originated amphibian LDD are discussed in the following sections. in the Amazon and Orinoco rivers and have been seen as far as 1,600 km out to ocean. Over the last Animals decades, rafting has been the most invoked means of Thienemann (1950) speculated that amphibian overwater LDD in amphibians, especially to explain the eggs could occasionally be carried in the plumage and occurrence of these animals on islands (e.g., Hedges on the feet and legs of aquatic birds. He also claimed 1996, Vences et al. 2003, Measey et al. 2007). In this that experiments conducted by Hesse (1924) revealed context, Kaiser et al. (1994) proposed the occurrence that the of some anurans can remain out of the of a natural mechanism, involving the combination of

Frontiers of Biogeography 2019, 11.4, e44577 © the authors, CC-BY 4.0 license 3 Fonte et al. Long-distance dispersal in amphibians floating rafts and favourable ocean currents that might use of complex models, which is beyond the scope of facilitate the dispersal of amphibians across oceans. this study. Measey et al. (2007) went further and proposed the existence of ‘freshwater paths’, a synergy of favourable Results ocean currents and the reduction of salinity in marine surface waters caused by the discharge of huge We found 70 articles, all published between 1960 amounts of freshwater from the mouths of large river and 2019, mentioning LDD in amphibians (references systems. Such a mechanism would enhance chances in Appendix S1). Only 3 studies (4%), published in of amphibian survival in rafts and was invoked to recent and all led by W.H. Lowe, have explicitly explain the occurrence of seven species (six anurans dealt with amphibian LDD, mainly exploring theoretical and one ) native to oceanic islands in the Gulf questions based on mark-and-recapture studies of of Guinea (Measey et al. 2007). salamanders in the field. The majority (68%) of LDD Anurans and even caecilians are commonly references recovered in our bibliographic search came found in floating meadow rafts in large river basins from molecular studies dealing with varied topics, (Achaval et al. 1979, Sarli et al. 1992, Schiesari et al. such as biogeographic, taxonomic, and phylogenetic 2003). Small invertebrates can also be found in rafts analyses. In these 48 studies, overwater jump dispersal (Donlan and Nelson 2003) and probably serve as was invoked as the most plausible explanation for a source of food for the vertebrates that share the present-day amphibian distributions when times flotsam. In journeys across oceans, fresh water could of divergence were not in agreement with be supplied by rainfall. Additionally, depending on geological histories, that is, when a vicariant origin the raft’s size and composition, it may even provide would require much older ages of the lineages than shelter from the sun. All things considered, rafting is what was in fact observed. Since taxon divergence the most plausible means of amphibian passive LDD, dates usually go back thousands or even millions especially for jump dispersal across oceans. of years, LDD events in these studies were inferred instead of observed. The first studies of this kind used allozyme (e.g., Busack 1986, Kaiser et al. 1994, Systematic review of the literature Toda et al. 1997) and albumin immunological data (e.g., Hedges et al. 1992, Hedges 1996). The more recent Methods studies used mainly mitochondrial and/or nuclear We performed a bibliographic search to compile DNA markers (e.g., Vences et al. 2003, Heinicke et al. information on how many studies have addressed 2007, Zimkus et al. 2017), sometimes coupled with LDD in amphibians, which methods were used, which analyses of morphological (e.g. Cannatella 2015) and taxa were involved, and when and where events had osteological (e.g., Martínez-Solano et al. 2004) characters. apparently occurred. In October 2018, we conducted a One study (Verneau et al. 2009) performed phylogenetic search in Web of Science (all databases/all years since analyses of parasites instead of their amphibian hosts. 1980/topic) and Scopus (all subject areas/all years to Thirty‑nine studies (55%) invoked natural overwater present/title, abstract, keywords) for scientific papers passive dispersal by means of rafting (Table 1), most of published in peer-reviewed journals containing the them to explain the occurrence of amphibian species following terms (and their plurals): long-distance or jump on islands (see below). Eleven studies (16%) invoked or oversea or overwater or over-water or transoceanic human-mediated overwater events, involving either or transmarine and dispersal and amphibia or anura intentional or accidental introductions. As mentioned or gymnophiona or caudata or urodela or frog or before, this kind of LDD is not the focus of our review salamander or newt or caecilian. Our search retrieved and will not be discussed. 146 publications. We excluded 29 that dealt with taxa other than amphibians and another 62 that did not Amphibian active LDD address LDD or whose definitions of LDD did not fit Based on LDD definitions and observations in the ours (see definitions below). We included another literature, we consider amphibian active LDD as the 15 published studies of our knowledge that were movement of individuals (adults, juveniles, or larvae) not listed in the results of these targeted searches. through the control of their own locomotion at longer Although most cases of overwater LDD were by distances than those on average involved in regular ancestral forms of extant amphibian species, in this movements (e.g., reproductive migration). This is review we refer to the currently living taxa. Taxonomy regardless of whether the movement leads to the follows Frost (2019). Distances involved in past LDD establishment of new populations and, consequently, events were estimated in the software GPlates v. 2.2 to a species’ geographic range expansion. Although (Müller et al. 2018) using maps obtained from the there are many exceptions (Smith and Green 2005), PALEOMAP PaleoAtlas (Scotese 2016). To estimate as a group, amphibians are predominantly site-loyal distances, we simply measured the shortest straight and of low vagility (Vences and Wake 2007). They line between places of origin and arrival at the geologic exhibit a wide range of dispersal strategies, and their time proposed in the studies. We consider this the dispersal capabilities suggest that occasional active minimum possible route and acknowledge that true migrants may connect populations separated by historical scenarios might have been more complex. tens of kilometres (Smith and Green 2005). It is clear However, obtaining higher accuracy would require the that different groups have different active dispersal

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Table1. Jump dispersal events recovered in a literature review on long-distance dispersal in amphibians. Extant taxon1 From – To When Method Reference CAUDATA Salamandridae Lyciasalamandra → Karpathos archipelago - allozymes, mtDNA Veith et al. 2008 billae Gutiérrez- Iberian Peninsula → Morocco ~ 0.24 Myr mtDNA, nuDNA Rodríguez et al. 2017 Pleurodeles waltl Spain – Morocco - allozymes Busack 1986 → Europe - mtDNA Veith et al. 2004 ANURA Alytidae Martinez-Solano et al. Alytes muletensis Iberian Peninsula → Balearic Islands ~ 3 Myr mtDNA, osteology 2004 Aromobatidae South America → Martinique < 11.3 Myr mtDNA, nuDNA Fouquet et al. 2013 chalcopis albumin immunological South America → Martinique 0 – 45 Myr Hedges 1996 data Bufonidae Spain – Morocco - allozymes Busack 1986 Bufo bufo between Baltic Sea islands2 recent, current allozymes Seppä and Laurila 1999 Oreophrynella proto-Andes → Pantepui3 ~ 38 Myr mtDNA, nuDNA Kok et al. 2017 Mainland ↔ West Indies ~ 51 Myr albumin Hedges et al. 1992 Peltophryne Hispaniola ↔ Cuba ~ 21.6 Myr albumin Hedges et al. 1992 guentheri Puerto Rico ↔ Hispaniola ~ 9.6 Myr albumin Hedges et al. 1992 Peltophryne Puerto Rico ↔ Hispaniola ~ 9.6 Myr albumin Hedges et al. 1992 Peltophryne Hispaniola ↔ Cuba ~ 21.6 Myr albumin Hedges et al. 1992 peltocephala Mainland ↔ West Indies ~ 51 Myr albumin Hedges et al. 1992 Peltophryne albumin immunological South America → West Indies 51 – 5.3 Myr Hedges 1996 peltocephalus Group4 data Craugastoridae Heinicke et al. 2007, Craugastor South America → 42 – 31 Myr mtDNA, nuDNA Hedges et al. 2008 Pristimantis South America → Lesser Antilles - allozymes Kaiser et al. 1994 euphronides Pristimantis shrevei South America → Lesser Antilles - allozymes Kaiser et al. 1994 Cycloramphidae mainland ↔ continental Thoropa taophora - nuDNA Duryea et al. 2015 islands Dicroglossidae Hoplobatrachus (north → south) recent mtDNA, nuDNA Sultana et al. 2016 tigerinus → - mtDNA Ewans et al. 2003 → Philippines - mtDNA Ewans et al. 2003 Philippines → Sulawesi - mtDNA Ewans et al. 2003 Limnonectes Sulawesi → Moluccas - mtDNA Ewans et al. 2003 Java/Bali → Lesser Sundas - mtDNA Ewans et al. 2003 Borneo → Sulawesi - mtDNA Ewans et al. 2003 South America → Greater Antilles 30.5 – 20.2 Myr mtDNA Duellman et al. 2016 (Hispaniola) Boana heilprini albumin immunological South America → West Indies - Hedges 1996 data 1Following Frost (2019); 2Possible active movements; 3Not referred to as overwater dispersal in the original publication; 4As in the original publication; 5Osteopilus brunneus in the original publication; 6Cited as Boophis n. sp. in Vences et al. (2003); 7Cited as n. sp. in Vences et al. (2003); 8Xenopus and Silurana in the original publication; 9Due to recent taxonomic changes, not possible to determine the species (cited as limnocharis in the original publication);10 Based on Hass and Hedges (1991); 11Based on Maxson and Heyer (1988); 12An alternative hypothesis proposed by the author involves normal overland dispersal (with subsequent extinction) across .

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Table1. Continued... Extant taxon1 From – To When Method Reference South America → Central America 17.3 – 11.3 Myr mtDNA Duellman et al. 2016 ebraccatus Dendropsophus South America → Central America 13.8 – 8.6 Myr mtDNA Duellman et al. 2016 microcephalus Group4 meridionalis Spain – Morocco - allozymes Busack 1986 Hyla savignyi → recent mtDNA Poulakakis et al. 2013 South America → Greater Antilles 26.1 – 17.3 Myr mtDNA Duellman et al. 2016 Osteopilus albumin immunological South America (?) → West Indies 48 – 5 Myr Hedges 1996 data Osteopilus Hispaniola ↔ Jamaica ~ 15.6 Myr albumin Hedges et al. 1992 dominicensis Hispaniola ↔ Cuba ~ 22.2 Myr albumin Hedges et al. 1992 Jamaica ↔ Cuba ~ 25.2 Myr albumin Hedges et al. 1992 Osteopilus ocellatus5 Hispaniola ↔ Jamaica ~ 15.6 Myr albumin Hedges et al. 1992 Mainland ↔ West Indies ~ 48 Myr albumin Hedges et al. 1992 Osteopilus Jamaica ↔ Cuba ~ 25.2 Myr albumin Hedges et al. 1992 septentrionalis Hispaniola ↔ Cuba ~ 22.2 Myr albumin Hedges et al. 1992 Hyperoliidae Africa → ~ 31 Myr mtDNA, nuDNA Pyron 2014 Heterixalus Africa → Madagascar 19 – 30 Myr mtDNA, nuDNA Vences et al. 2003 Hyperolius West-Central Africa → São Tomé 8.9 – 3.4 Myr mtDNA, nuDNA Bell et al. 2015a São Tomé → Príncipe 1.1 – 0.27 Myr mtDNA, nuDNA Bell et al. 2015a Hyperolius molleri São Tomé → Príncipe - mtDNA, nuDNA Bell et al. 2015b Africa → Madagascar ~ 31 Myr mtDNA, nuDNA Pyron 2014 Tachycnemis Madagascar → 11 – 21 Myr mtDNA, nuDNA Vences et al. 2003 Tachycnemis Madagascar → Seychelles 11 – 19 Myr mtDNA, nuDNA Maddock et al. 2014 seychellensis Madagascar → Seychelles 9.79 – 35.34 Myr nuDNA Crottini et al. 2012 Eleutherodactylidae South America → Lesser Antilles ~ 20 Myr mtDNA, nuDNA Heinicke et al. 2007 Eleutherodactylinae Hispaniola/Puerto Rico → Lesser ~ 20 Myr mtDNA, nuDNA Heinicke et al. 2007 Antilles Heinicke et al. 2007, Eleutherodactylus South America → West Indies 47 – 29 Myr mtDNA, nuDNA Hedges et al. 2008 Mainland ↔ West Indies ~ 37.2 Myr albumin Hedges et al. 199210 Eleutherodactylus Jamaica ↔ Cuba ~ 24.6 Myr albumin Hedges et al. 199210 gossei Hispaniola ↔ Jamaica ~ 22.8 Myr albumin Hedges et al. 199210 Mainland ↔ West Indies ~ 37.2 Myr albumin Hedges et al. 199210 Eleutherodactylus Jamaica ↔ Cuba ~ 24.6 Myr albumin Hedges et al. 199210 nubicola Hispaniola ↔ Jamaica ~ 22.8 Myr albumin Hedges et al. 199210 Eleutherodactylus Hispaniola ↔ Jamaica ~ 22.8 Myr albumin Hedges et al. 199210 pictissimus Hispaniola ↔ Cuba ~ 22.2 Myr albumin Hedges et al. 199210 Mainland ↔ West Indies ~ 37.2 Myr albumin Hedges et al. 199210 Eleutherodactylus Jamaica ↔ Cuba ~ 24.6 Myr albumin Hedges et al. 199210 planirostris Hispaniola ↔ Cuba ~ 22.2 Myr albumin Hedges et al. 199210 Eleutherodactylus Heinicke et al. 2007, Cuba → North America ~ 19 Myr mtDNA, nuDNA (Syrrhophus)4 Hedges et al. 2008 Eleutherodactylus (Euhyas) luteolus Cuba → Jamaica - mtDNA, nuDNA Hedges et al. 2008 Species Series4 Eleutherodactylus (Euhyas) ricordii Cuba ↔ Hispaniola - mtDNA, nuDNA Hedges et al. 2008 Species Series4 Leptodactylidae 1Following Frost (2019); 2Possible active movements; 3Not referred to as overwater dispersal in the original publication; 4As in the original publication; 5Osteopilus brunneus in the original publication; 6Cited as Boophis n. sp. in Vences et al. (2003); 7Cited as Mantidactylus n. sp. in Vences et al. (2003); 8Xenopus and Silurana in the original publication; 9Due to recent taxonomic changes, not possible to determine the species (cited as Rana limnocharis in the original publication);10 Based on Hass and Hedges (1991); 11Based on Maxson and Heyer (1988); 12An alternative hypothesis proposed by the author involves normal overland dispersal (with subsequent extinction) across Antarctica.

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Table1. Continued... Extant taxon1 From – To When Method Reference Mainland ↔ West Indies ~ 39.6 Myr albumin Hedges et al. 199211 albumin immunological Leptodactylus South America → West Indies 40 – 4.5 Myr Hedges 1996 data albilabris Hedges and Heinicke South America → West Indies 24 – 58 Myr mtDNA 2007 Hedges and Heinicke South America → West Indies 23 – 34 Myr mtDNA 2007 Leptodactylus fallax albumin immunological South America → Lesser Antilles 3 – 7 Myr Hedges 1996 data Leptodactylus albumin immunological Central/South America → West Indies 0 – 2 Myr Hedges 1996 insularum data South America → Trinidad ~ 1 Myr mtDNA Camargo et al. 2009 South America → Tobago ~ 220 Ka mtDNA Camargo et al. 2009 Leptodactylus validus Trinidad → Lesser Antilles 400 – 117 Ka mtDNA Camargo et al. 2009 albumin immunological South America → West Indies 0 – 2 Myr Hedges 1996 data Madagascar → Mayotte < 8.7 Myr mtDNA, nuDNA Vences et al. 2003 Boophis nauticus6 mtDNA, morphology, Madagascar → Mayotte - Glaw et al. 2019 bioacoustic Madagascar → Mayotte < 8.7 Myr mtDNA, nuDNA Vences et al. 2003 Blommersia mtDNA, morphology, transmarina7 Madagascar → Mayotte - Glaw et al. 2019 bioacoustic Micrixalidae Micrixalus Africa → South Asia ~ 29 Myr mtDNA, nuDNA Pyron 2014 Africa → Madagascar ~ 66 Myr nuDNA Feng et al. 2017 Microhylidae Africa → South America ~ 66 Myr nuDNA Feng et al. 2017 Papuan peninsula → - mtDNA, nuDNA Oliver et al. 2013 Louisiade archipelago Mantophryne Papuan peninsula → D’Etrecasteaux - mtDNA, nuDNA Oliver et al. 2013 archipelago South America → 61 – 52 Myr mtDNA, nuDNA Pyron 201412 Agalychnis South America → Central America 12.3 – 7.9 Myr mtDNA Duellman et al. 2016 Pipidae Xenopus8 South America → Africa 40 – 75 Myr nuDNA, morphology Cannatella 2015 Ptychadenidae Africa → Madagascar - mtDNA Vences et al. 2004 Ptychadena molecular analysis of Africa → Madagascar 14.2 – 2.3 Myr Verneau et al. 2009 mascareniensis parasites East Africa → Madagascar ~ 15.5 Myr mtDNA, nuDNA Zimkus et al. 2017 East Africa → São Tomé - mtDNA Measey et al. 2007 Ptychadena newtoni Africa → São Tomé ~ 11.4 Myr mtDNA, nuDNA Zimkus et al. 2017 Ranidae Amnirana → Africa ~ 18.7 Myr mtDNA, nuDNA Oliver et al. 2015 New Guinea → Solomon and Papurana kreffti ~ 2.98 Myr mtDNA, nuDNA Oliver et al. 2015 Bismarck Islands Pelophylax bedriagae Middle East → Cyprus ~ 1.65 Myr mtDNA Poulakakis et al. 2013 1Following Frost (2019); 2Possible active movements; 3Not referred to as overwater dispersal in the original publication; 4As in the original publication; 5Osteopilus brunneus in the original publication; 6Cited as Boophis n. sp. in Vences et al. (2003); 7Cited as Mantidactylus n. sp. in Vences et al. (2003); 8Xenopus and Silurana in the original publication; 9Due to recent taxonomic changes, not possible to determine the species (cited as Rana limnocharis in the original publication);10 Based on Hass and Hedges (1991); 11Based on Maxson and Heyer (1988); 12An alternative hypothesis proposed by the author involves normal overland dispersal (with subsequent extinction) across Antarctica.

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Table1. Continued... Extant taxon1 From – To When Method Reference China → Ryukyu archipelago ↔ Fejervarya sp.9 - allozymes Toda et al. 1997 Japan main islands Rana temporaria between Baltic Sea islands2 recent, current allozymes Seppä and Laurila 1999 Luzon → Mindanao ~ 7.3 Myr mtDNA, nuDNA Brown et al. 2016 Sanguirana Luzon → Western Visayas ~ 5.9 Myr mtDNA, nuDNA Brown et al. 2016 Amami → Tokara Archipelago 0.1 – 2.9 Myr mtDNA Tominaga et al. 2015 Amami → Takara ~ 24.8 Ka mtDNA, nuDNA Komaki et al. 2017 Buergeria japonica Takara → Taira ~ 9.1 Ka mtDNA, nuDNA Komaki et al. 2017 Taira → Naka ~ 4.6 Ka mtDNA, nuDNA Komaki et al. 2017 Naka → Kuchi ~ 1.8 Ka mtDNA, nuDNA Komaki et al. 2017 1Following Frost (2019); 2Possible active movements; 3Not referred to as overwater dispersal in the original publication; 4As in the original publication; 5Osteopilus brunneus in the original publication; 6Cited as Boophis n. sp. in Vences et al. (2003); 7Cited as Mantidactylus n. sp. in Vences et al. (2003); 8Xenopus and Silurana in the original publication; 9Due to recent taxonomic changes, not possible to determine the species (cited as Rana limnocharis in the original publication);10 Based on Hass and Hedges (1991); 11Based on Maxson and Heyer (1988); 12An alternative hypothesis proposed by the author involves normal overland dispersal (with subsequent extinction) across Antarctica. characteristics and capabilities (larvae vs. juveniles vs. LDD events found in our literature search to be jump adults; anurans vs. salamanders vs. caecilians; terrestrial dispersal (Table 1, Fig. 1). We recovered at least 87 events vs. aquatic vs. arboreal vs. fossorial; pond‑breeding involving at least 53 extant species and 36 extant genera vs. direct development; etc.) and that different reported in 38 studies. The majority of events (84) features of the landscape can affect the success of involved anurans (51 species) and only 3 salamanders such movements. Because of these differences, it is (2 species). Although no study reported LDD events for difficult to assign a threshold over which a movement caecilians, the occurrence of an endemic species on a should be considered long-distance. Despite this, continental island ( thomense in São the few studies that have compiled information on Tomé, Gulf of Guinea) was suggested by Measey et al. amphibian movement distances (e.g., Marsh and (2007) to be the result of transoceanic dispersal by Trenham 2001, Smith and Green 2005) have shown that, means of rafting, that is, jump dispersal. in general, amphibians rarely travel distances greater Even though most cases of jump dispersal reported than 10 km. Smith and Green (2005) found that the in the literature (Table 1) involve the colonization of average maximum movement recorded for anurans islands (see below), there are also suggestions of is 2.02 km and suggested that for both salamanders movements between continental landmasses separated and anurans population differentiation is most likely by oceans and seas, such as between Africa and to occur at scales upward of 10 km. Thus, we here Europe (Bufo bufo, Hyla meridionalis, Busack 1986; propose that 10 km is a reasonable threshold for an Pleurodeles waltl, Busack 1986, Veith et al. 2004, active amphibian movement to be considered LDD. Gutiérrez‑Rodríguez et al. 2017), Africa and South America (Xenopus spp., Cannatella 2015; microhylids, Feng et al. Amphibian passive LDD 2017), Africa and South Asia (Micrixalus, Pyron 2014) Based on LDD definitions and observations in and South America and Central America (Craugastor, the literature, we use the following definition for Heinicke et al.2007, Hedges et al.2008; Agalychnis, passive LDD in amphibians. Individuals travel passively Dendropsophus ebraccatus, D. gr. microcephalus, (movement occurs outside of their own control) over Duellman et al. 2016). longer distances than those involved in regular active movements, regardless of whether this leads to the Amphibians on islands establishment of new populations and, consequently, to Usually, two competing biogeographic views are a species’ geographic range expansion. This can apply invoked to explain the presence of amphibians on to individuals at any life stage, from eggs to adults. islands: (i) populations were continuously distributed Jump dispersal, in contrast, requires the successful before island formation and were subsequently isolated establishment of a population (cf. Pielou 1979). following the splitting of land masses and/or the rise Following the same criteria we used for active LDD of water levels; (ii) populations were introduced by (see above), we propose that 10 km is an appropriate humans or naturally established by dispersal, either minimum distance for a passive amphibian movement normal active dispersal across previous land connections to be considered LDD. or via jump dispersal. The region has proven to be the ideal Jump dispersal natural laboratory to test these alternative hypotheses. Even though only 5 studies explicitly used this Working in this region, based on molecular data, term, we consider all of the natural overwater passive Hedges et al. (1992) were pioneers in providing scientific

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Figure 1. Schematic map showing regions where most long-distance dispersal events of amphibians retrieved in our bibliographic search appear to have occurred. 1 = West Indies and surroundings; 2 = Mediterranean Sea, Iberian Peninsula; 3 = Mediterranean Sea, Middle East; 4 = Gulf of Guinea; 5 = Madagascar, and Seychelles; 6 = Philippine Sea; 7 = Solomon and Bismarck archipelagos. For detailed information about these events, seeTable 1. evidence that amphibians might have colonized In our bibliographic search, we found 30 studies islands via overwater dispersal instead of via ancient reporting at least 73 jump dispersal events that resulted land connections. Hedges (1996) went further and, in the colonization of at least 39 islands by at least challenging the popular vicariance paradigm, proposed 42 extant amphibian species and 25 genera (Table 1). that ancestors of most of the extant Caribbean The majority of cases (54%) come from the West Indies amphibian fauna arrived on the islands attached to region. This can be explained both by the high diversity flotsam following water currents originating in South of endemic amphibian species on these islands and America. Further studies (Hedges and Heinicke 2007, the large number of studies conducted in the region. Heinicke et al. 2007, Hedges et al. 2008, Duellman et al. Also worth noting are the studies conducted in Africa 2016) not only confirmed previous LDD predictions (Gulf of Guinea, Comoros, Seychelles and Madagascar), but also included other taxa and refined dates of the Pacific Ocean (Tokara, Ryukyu, Philippine, Solomon dispersal events. and Bismarck archipelagos), and the Mediterranean Regarding continental islands, sometimes normal Sea (Cyprus and the Balearic islands) (Table 1, Fig. 1). dispersal across former land bridges (e.g. O’Connel et al. 2018) and previous occurrence before island formation Distances (e.g., Lourenço et al. 2018, Martinez-Solano and Lawson We found only 3 studies that recorded amphibian 2009) were invoked to explain amphibian occurrence. active movements at distances greater than 10 km, In other cases, such as in Madagascar, transoceanic all involving adult bufonid toads, namely Anaxyrus jump dispersal from Africa, with subsequent species‑rich fowleri (34 km, Smith and Green 2006), A. boreas radiations into the rainforests, was invoked to explain the (13 km, Schmetterling and Young 2008), andRhinella highly endemic amphibian fauna of the island (Vences marina (21.8 km, Phillips et al. 2007). 2004). With respect to the presence of amphibians on Concerning passive LDD, given the high degree of oceanic islands, until recently researchers believed that uncertainty surrounding these events, only a couple it was the result of human translocations (Vences et al. of studies have attempted to speculate about the 2003). Recent molecular studies have shown, however, distances travelled. To calculate reliable estimates of that divergence times of island and mainland species these distances, one would have to know – with relatively are much deeper than the origin of humans, leaving high accuracy – the timing of the event, the geological natural jump dispersal as the only possible explanation conformation of the region at that time (including sea for amphibian occurrence on these islands. levels, direction of ocean currents, possible existence

Frontiers of Biogeography 2019, 11.4, e44577 © the authors, CC-BY 4.0 license 9 Fonte et al. Long-distance dispersal in amphibians of land/ice connections and stepping stone islands, Although our results demonstrate that LDD via etc.), and the approximate points of origin and arrival. rafting can indeed involve long journeys across Unfortunately, for most cases, this information is not oceans, it does not necessarily mean that amphibians available or is not accurate enough. In fact, out of covered these distances in just one trip. Tectonic 87 jump dispersal events recovered in our bibliographic processes and past fluctuations in sea levels have search (Table 1), only 12 meet these requirements. constantly increased and decreased land areas, with For the remaining cases, the age estimates of events many potential stepping‑stone islands emerging and are not precise enough (or were not estimated at all), subsiding over time. Because of that, we cannot rule the origin and destination points are too generic (e.g., out that these journeys were in fact completed in from Africa to South America) or events occurred in multiple shorter steps. places with complicated and still unsolved geological histories, such as the Caribbean region (for a review General conclusions of the different geological hypotheses for this region, Although the distribution patterns of major amphibian see James et al. 2009). Nevertheless, some cases are lineages are mainly explained by a Pangean origin worth discussing. with subsequent vicariant diversification following the In the Mediterranean Sea, LDD events generally Laurasian and Gondwanan fragmentation, extinction appear to have occurred over shorter distances than and dispersal events have also exerted a strong influence in other regions. Gutiérrez-Rodríguez et al. (2017) suggested that the salamander Pleurodeles waltl may on present-day distributions (Vences and Köhler 2008, have rafted from the Iberian Peninsula to Morocco, Pyron 2014). Despite the substantial evidence for covering distances between 3.5 and 14.4 km across the dispersal that we have presented in this review, it would Strait of Gibraltar. Poulakakis et al. (2013) proposed that still be premature to conclude that dispersal is more the ranid frog Pelophylax bedriagae colonized Cyprus important than vicariance in explaining distributions from the Middle East mainland crossing distances of broken up by oceans (de Queiroz 2005). Yet, we have at least 30 km over the sea. Martinez-Solano et al. shown that overwater jump dispersal events have played (2004) argued that the ancestor of the toad Alytes an important role in generating current amphibian muletensis must have reached the Balearic Islands biogeographic patterns, especially the occurrence of through a transmarine colonization process from the disjunct distributions and the colonization of islands. Iberian Peninsula. Our calculations in GPlates estimate distances at 150–250 km for this LDD event. Acknowledgments Distances crossed in the region were LFMF thanks Alan de Queiroz for fruitful discussions considerably longer. We recovered at least 4 LDD events and A. Elbakyan for her work. We thank Robert J. from the African mainland to Madagascar (Heterixalus, Whittaker, L. R. Heaney, and an anonymous reviewer Vences et al. 2003, Pyron 2014; Tachycnemis, Pyron 2014; Ptychadena mascareniensis, Verneau et al. for their valuable suggestions on a first version of 2009, Zimkus et al. 2017; Microhylidae, Feng et al. this manuscript, and Susan Kennedy for her kind help Coordenação de 2017). Our calculations in GPlates estimate distances with the English revision. We thank at 350–500 km for these events, depending on the Aperfeiçoamento de Pessoal de Nível Superior (CAPES), geologic time at which they occurred. Furthermore, German Academic Exchange Service (DAAD), and Trier Vences et al. (2003) suggested that mantellid frogs University, for funding of LFMF. MM benefited from (Boophis nauticus and Blommersia transmarina; a doctorate fellowship by Konrad-Adenauer-Stiftung cf. Glaw et al. 2019) dispersed from Madagascar to (KAS). LFMF dedicates this work to the memory of Mayotte in Comoros crossing distances of at least Rafael C. Bortolin. 250 km over the sea. Still, the most enlightening cases come from the Author contributions Gulf of Guinea in the Atlantic Ocean. Measey et al. All authors developed the idea of this study and (2007) suggested that the frog Ptychadena newtoni contributed equally to discussions. LFMF led the reached São Tomé island in rafts leaving the mouth of bibliographic search and analysis with support of MM. the Congo River in western Central African mainland, The manuscript was written by LFMF with input from SL. covering distances of around 1,000 km across the ocean. A similar pattern was proposed to explain the presence Supplementary Materials of hyperoliid frogs (Hyperolius) in the Gulf of Guinea. Bell et al. (2015a,b) suggested that these amphibians The following materials are available as part of reached São Tomé via rafts originated either in the mouth the online article from https://escholarship.org/uc/fb of the Congo or the Ogooué rivers (1,000 and 250 km Appendix S1. List of 70 studies recovered in the from the island, respectively) and further dispersed bibliographic search on long-distance dispersal in over 150 km to its neighbour island Príncipe. amphibians.

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References de Queiroz, A. (2005) The resurrection of oceanic dispersal in historical biogeography. Trends Achaval, F., González, J.G., Meneghel, M. & Melgarejo, in Ecology and , 20, 68–73. A.R. (1979) Lista comentada del material recogido em costas uruguayas, transportado improbable journeys shaped the history of por camalotes desde el Rio Parana. Acta de Queiroz, A. (2014) The Monkey’s voyage: how Zoologica Lilloana, XXXV, 195–200. Barber, H.N., Dadswell, H.E. & Ingle, H.D. (1959) thelife. move.Basic Books,Oxford NewUniversity York. Press, Oxford. Transport of driftwood from South America Donlan,Dingle, H. C.J. (1996) & Nelson, Migration: P.A. (2003) the biology Observations of life onof to Tasmania and Macquarie Island. Nature, 184, 203–204. Bulletininvertebrate of Marine colonized Science, flotsam 72, in231–240. the eastern Kielgast, J., Lötters S., Stuart B.L. & Zamudio, Duellman,Tropical W.E., Pacific, Marion, with A.B. a & discussion Hedges, S.B. of rafting.(2016) Bell, R.C.,K.R. Drewes,(2015a) OverseasR.C., Channing, dispersal A., of Gvoždík, Hyperolius V., reed frogs from Central Africa to the oceanic Zootaxa,, 4104, classification, 1–109. and biogeography Biogeography, 42, 65–75. Elsom,of D. the (1988) treefrogs Catch (Amphibia: a falling frog. Anura: New Arboranae). Scientist, islands of São Tomé and Príncipe. Journal of Bell, R.C., Drewes, R.C. & Zamudio, K.R. (2015b) 1615, 129–131. Fahr, J. (1993) Ein Beitrag zur Biologie der Amphibien overseas dispersal, the progression rule, and der Insel São Tomé (Golf von Guinea) (Amphibia). inReed situ frog speciation. diversification Evolution, in the 69, Gulf 904–915. of Guinea: Faunistische Abhandlungen, 19, 75–84. Bossuyt, F., Brown, R.M., Hillis, D.M., Cannatella,

and biogeography of a cosmopolitan frog Feng, PhylogenomicsY.J., Blackburn, revealsD.C., Liang, rapid, D., simultaneous Hillis, D.M., D.C. & Milinkovitch, M.C. (2006) Phylogeny Wake, D.B., Cannatella, D.C. & Zhang, P. (2017) resulted in continent-scale endemism in Gondwanan frogs at the -Paleogene theradiation: family Ranidae.late Cretaceous Systematic diversification Biology, 55, boundary.diversification Proceedings of three of the major National Academy of 579–594. of Sciences USA, 114, E5864-E5870.

herpetofauna separated by the formation of an online reference (version 6.0, accessed in Busack,the S.D. Strait (1986) of Gibraltar. Biogeographic National analysis Geographic of the Frost, 13D.R. May (2019) 2019). Amphibian American species Museum of theof Natural world: Research, 2, 17–36. Cannatella, D. (2015) Xenopus History, New York, USA. Electronic Database fossils, node calibrations, tip-dating, and in space and time: accessible at http://research.amnh.org/ paleobiogeography. Cytogenetic and Genome /amphibia/index.html. Research, 145, 283–301. Glaw, F.,island Hawlitschek, frogs and O., Glaw,transmarine K. & Vences, dispersal M. (2019) of amphibiansIntegrative evidencebetween Madagascar confirms new and endemic Mayotte (ed.) (2012) Dispersal ecology and evolution. Clobert, J., Baguette, M., Benton, T.G. & Bullock, J.M. (Comoros archipelago). The Science of Nature, Oxford University Press, Oxford. 106, 1–14. Croizat, L., Nelson, G. & Rosen, D.E. (1974) Centers of origin and related concepts. Systematic Solano, I. (2017) Integrative inference of , 23, 265–287. Gutiérrez-Rodríguez,population history J., Barbosa, in the Ibero-Maghrebian A.M. & Martínez- Darlington, P.J. (1938) The origin of the fauna of the endemic Pleurodeles waltl (Salamandridae). Greater Antilles, with discussion of dispersal Molecular Phylogenetics and Evolution, 112, of animals over water and through the air. The 122–137. Quarterly Review of Biology, 13, 274–300. Halstead, L.B. (1980) Museum of errors. Nature, Darwin, C. (1859) by means 288, 208. of or the preservation of Hass, C.A. & Hedges, S.B. (1991) Albumin evolution in favoured races in the struggle for life. John West Indian frogs of the Eleutherodactylus Murray, London.

Frontiers of Biogeography 2019, 11.4, e44577 (Leptodactylidae):© the authors, Caribbean CC-BY 4.0biogeography license 11 Fonte et al. Long-distance dispersal in amphibians

and a calibration of the albumin immunological

Hedges, S.B. (1996) The origin of West Indian Kraus,Nature, F. (2009) Basel. Alien reptiles and amphibians: a clock. Journal of Zoology, 225, 413–416. scientific compendium and analysis. Springer G. (2018) Role of colonization history and Albertamphibians Schwartz and (ed.reptiles. by R. In: Powell Contributions and R.W. Lourenço, A., Sequeira, F., Buckley, D. & Velo-Antón, Henderson),to West Indian pp. 95–128. herpetology: Society Afor tribute the Study to of two salamander species inspecies-specific a island-mainland traits on contemporary system. Journal Hedges, S.B., Hass, C.A. & Maxsom, L.R. (1992) of Biogeography, 45, 1054–1066. of Amphibians and Reptiles, New York. Marsh, D.M. & Trenham, P.C. (2001) Metapopulation for dispersal in West Indian terrestrial dynamics and amphibian conservation. vertebrates.Caribbean biogeography: Proceedings molecular of the National evidence Conservation Biology, 15, 40–49. Academy of Sciences USA, 89, 1909–1913.

Martínez-Solano, I. & Lawson, R. (2009) Escape phylogeny and biogeography of West Indian salamanders (Batrachoseps) on the islands to Alcatraz: evolutionary history of slender Hedges,frogs S.B. of & the Heinicke, genus M.P.Leptodactylus (2007) Molecular (Anura, of San Francisco Bay. BMC Evolutionary Leptodactylidae). Molecular Phylogenetics Biology, 9, 38. and Evolution, 44, 308–314.

Martínezrelationships‐Solano, I., andGonçalves, biogeography H.A., Arntzen, of midwife J.W. Hedges, S.B., Duellman, W.E. & Heinicke, M.P. (2008) & García‐París, M. (2004)Alytes Phylogenetic). Journal of biogeography,New World direct-developing and conservation. frogs Zootaxa, (Anura: Biogeography, 31, 603–618. toads (Discoglossidae: 1737,Terrarana): 1–182. molecular phylogeny, classification,

Mattysen,(ed. E.by (2012) J. Clobert, Multicausality M. Baguette, of T.G.dispersal: Benton a Major Caribbean and Central American frog review. In: Dispersal ecology and evolution Heinicke,faunas M.P., originated Duellman, by W.E. ancient & Hedges, oceanic S.B. dispersal. (2007) Press, Oxford. Proceedings of the National Academy of and J.M. Bullock), pp. 3–18. Oxford University Sciences USA, 104, 10092–10097. Maxson, L.R. & Heyer, W.R. (1988) Molecular of the frog genus Leptodactylus Grundlage. Gustav Fischer, Jena. Hesse, R. (1924) Tiergeographie auf ökologischer Zoology, 41, 1–13. McAtee,(Amphibia: W.L. (1917) Leptodactylidae). Showers of organic Fieldiana matter. Monthly Weather Review, 45, 217–224. Hopkins,evolutionary G.R. & Brodie, perspective. E.D. (2015) Herpetological Occurrence of Monographs,amphibians in 29, saline 1–27. habitats: a review and James, K.H., Lorente, M.A. & Pindell, J.L. (2009) The Measey,amphibian G.J., Gower, D.J, Oommen, ramaswamii O.V. & Wilkinson, M. origin and evolution of the Caribbean Plate. (2003) A mark-recapture study of the caecilian The Geological Society, London. Journal of Zoology, 261, 129–133. (Amphibia: Jordano, P. (2017) What is long-distance dispersal? Gymnophiona: ) in southern . And a taxonomy of dispersal events. Journal M. & Bourles, B. (2007) Freshwater paths of Ecology, 105, 75–84. Measey, G.J., Vences, M., Drewes, R.C., Chiari, Y., Melo, Kaiser, H., Sharbel, T.F. & Green, D.M. (1994) Systematics frog Ptychadena newtoni gives insights into and biogeography of eastern Caribbean amphibianacross the ocean: colonization molecular of phylogenyoceanic islands. of the Eleutherodactylus Journal of Biogeography 34, 7–20. evidence from allozymes. Amphibia–Reptilia, Müller, R.D., Cannon, J., Qin, X., Watson, R.J., Gurnis, 15, 375–394. (Anura: Leptodactylidae): M., Williams, S., Pfaffelmoser, T., Seton, M., Kleyheeg, E. & Van Leeuwen, C.H.A. (2015) Regurgitation Building a virtual Earth through deep time. long-distance dispersal of wetland plant seeds. Geochemistry,Russel, S.H.J. & Geophysics,Zahirovic, S. Geosystems,(2018) GPlates: 19, Aquaticby waterfowl: Botany, an 127, overlooked 1–5. mechanism for 2243–2261.

Frontiers of Biogeography 2019, 11.4, e44577 © the authors, CC-BY 4.0 license 12 Fonte et al. Long-distance dispersal in amphibians

of Pangaea. The American Naturalist, 165, 590–599. Nathan,Diversity R. (2005) and Long-distance Distributions, dispersal 11, 125–130. research: Sarli, V., Santos, M., Maneyro, R. & Achaval, F. (1992) Nathan,building R. (2006) a networkLong-distance of yellow dispersal brick of plants.roads. Nuevos aportes sobre la fauna arribada a las Science, 313, 786–788. costas uruguayas em balsas de camalotes.

on the history of biogeography. Journal of the 7, 77–78. Nelson,History G. (1978) of FromBiology, Candolle 11, 269–305. to Croizat: comments Schiesari,Boletín L., Zuanon, de la Sociedad J., Azevedo–Ramos, Zoológica del C., Uruguay, Garcia, M., Gordo, M., Messias, M., Vieira, E.M. (2003)

Nelson, G. & Platnick, N. (1981) Systematics and and amphibians in the lower Solimões River, Biogeography: cladistics and vicariance. CentralMacrophyte Amazon. rafts as Journal dispersal of Tropical vectors for Ecology, fishes Kurniawan,Columbia University N. & Fujita, Press, M.K. New (2018) York. Within- 19, 333–336. O’Connell, K.A., Smart, U., Smith, E.N., Hamidy, A., frog (Rhacophorus) species accumulation on movements of boreal toads (Bufo boreas boreas) theisland Sunda diversification Shelf. Journal underlies of Biogeography, parachuting 45, Schmetterling,in two western D.A. & Young,Montana M.K. basins. (2008) Journal Summer of 929–940. Herpetology, 42, 111–123. Phillips, B.L., Brown, G.P., Greenlees, M., Webb, J.K. & Schuchert, C. (1935) Historical geology of the Shine, R. (2007) Rapid expansion of the cane Antillean-Caribbean region. Wiley & Sons, toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology, 32, 169–176. Scotese, C.R. (2016) PALEOMAP PaleoAtlas for Pielou, E.C. (1979) Biogeography. John Wiley, New GPlatesNew York. and the Paleo Data Plotter Program,

York. PALEOMAP Project. Available at: https:// Poulakakis, N., Kapli, P., Kardamaki, A., Skourtanioti, www.earthbyte.org/paleomap-paleoatlas- phylogeographyE., Göcmen, B., Ilgaz, of six C.,herpetofauna Kumlutaş, Y.,species Avci, for-gplates/ (accessed in 10 September 2019) A. & Lymberakis, P. (2013) Comparative Shigesada, N. & Kawasaki, K. (2002) Invasion and colonization routes. Biological Journal of the the range expansion of species: effects of Linneanin Cyprus: Society, Late 108, 619–635. to Pleistocene Hails),long-distance pp. 350–373. dispersal. Cambridge In: Dispersal University ecology Pyron, R.A. (2014) Biogeographic analysis reveals (ed. by J.M. Bullock, R.E. Kenward and R.S. ancient continental vicariance and recent Smith, M.A. & Green, D.M. (2005) Dispersal and oceanic dispersal in amphibians. Systematic Press, New York. Biology, 63, 779–797. the metapopulation paradigm in amphibian Roelants, K. & Bossuyt, F. (2005) Archaeobatrachian populations metapopulations? Ecography, 28,ecology 110–128. and conservation: are all amphibian crown-group frogs. Systematic Biology, 54, 111–126. and Pangaean diversification of Smith, M.A. & Green, D.M. (2006) Sex, isolation and

stone? Ten questions about dispersal evolution. terrestrial amphibian. Ecography, 29, 649–658. fidelity: unbiased long-distance dispersal in a Ronce,Annual O. (2007) Review How does of Ecology, it feel to Evolution,be like a rolling and Systematics, 38, 231–253. Stoddart,and D.R. Environment, (1981) Biogeography: 5, 575–590. dispersal and Thienemann,drift. Progress A. (1950) in VerbreitungsgeschichtePhysical Geography: Earth der Rosen,Systematics D.E. (1981) Discussion Introduction. Group ofIn: the vicariance American Süßwassertierwelt Europas. Versuch einer Museumbiogeography: of Natural a critique. History Symposium (ed. by G. Nelson of the historischen Tiergeographie der europäischen and D.E. Rosen), pp. 1–5. Columbia University Binnengewässer. Schweizerbart‘sche Verlagsbuchhandlung, Stuttgart. San Mauro, D., Vences, M., Alcobendas, M., Zardoya, Toda, M., Nishida, M., Matsui, M., Wu. G.F. & Ota, H. Press, New York. (1997) Allozyme variation among East Asian populations of the Indian rice frog Rana R. & Meyer, A. (2005) Initial diversification Frontiersof of living Biogeography amphibians 2019, 11.4, predated e44577 the breakup © the authors, CC-BY 4.0 license 13 Fonte et al. Long-distance dispersal in amphibians

limnocharis Verneau, O., Du Preez, L.H., Laurent, V., Raharivololoniaina, Systematics and Ecology, 25, 143–159. L., Glaw, F. & Vences, M. (2009) The double Veith, M., Mayer, C., (Amphibia: Samraoui, Anura). B., Barroso, Biochemical D.D. & Bogaerts, S. (2004) From Europe to Africa and leads to new insights on the origins of their amphibianodyssey of Madagascan hosts. Proceedings polystome of flatwormsthe Royal dispersal in ribbed salamanders (genus Society B, 276, 1575–1583. Pleurodelesvice versa: evidence). Journal for multiple of Biogeography, intercontinental 31, Wells, K.D. (2007) The ecology and behavior of 159–171. amphibians. University Of Chicago Press, Chicago. A perspective from amphibians, reptiles and Zeisset, I. & Beebe, T.J.C. (2008) Amphibian Vences, M. (2004) Origin of Madagascar’s extant fauna: of Zoology, 71, 217–228. historical aspects of species distributions. other non‐flying vertebrates. Italian Journal Heredity,phylogeography: 101, 109–119. a model for understanding Kosuch, J., Veith, M. & Meyer, A. (2003) Multiple Vences,overseas M., Vieites, dispersal D.R., in Glaw, amphibians. F., Brinkmann, Proceedings H., of the Royal Society B, 270, 2435–2442. Zimkus, B.M., Lawson, L.P., Barej, M.F. et al. (2017) MadagascarLeapfrogging to into maintain new territory: their ecological how Mascarene niche. boundaries and phylogeography of amphibians. Molecularridged frogs Phylogenetics diversified and across Evolution, Africa 106,and Vences, M. & Wake, D.B. (2007) Speciation, species 254–269. H.H. Heatwole and M. Tyler), pp. 2613–2669. SurreyIn: Amphibian Beatty &Biology, Sons, Chipping 6, Systematics Norton. (ed. by Submitted: 18 July 2019 Vences, M. & Köhler, J. (2008) Global diversity First decision: 23 August 2019 of amphibians (Amphibia) in freshwater. Accepted: 1 October 2019 Hydrobiologia, 595, 569–580. Edited by Robert J. Whittaker

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