2632  |  wileyonlinelibrary.com/journal/jbi Journal of Biogeography. 2019;46:2632–2636.© 2019 John Wiley & Sons Ltd

Received: 9 April 2019  |  Revised: 28 May 2019  |  Accepted: 7 June 2019

DOI: 10.1111/jbi.13659

C O R R E S P O N D E N C E

Mammals and long‐distance over‐water colonization: The case for rafting dispersal; the case against phantom causeways

AbstractIn the absence of evidence suggesting former ice or land bridges, the colonization of remote landmasses by non‐aquatic, non‐fly‐ing vertebrates is thought to result from long‐distance over‐water rafting (LDOR). However, Mazza et al. (2019) challenge the no‐tion that mammals can make such journeys citing their perceived physiological inadequacies. They claim that lengthy transits com‐bined with lack of food and water plus the stresses imposed by temperature, humidity and salinity render such passages impos‐sible. We, though, contend that this reasoning is wrong. The few cases where LDOR has been invoked for mammal colonization have all involved small‐bodied animals, several of which are able to drastically reduce their metabolic rates through torpor/hiber‐nation when food and water are scarce. Furthermore, there may be sustenance. Crucially, LDOR obviates the need for miraculous short‐lived causeways and the attendant issue of unrecognized large‐scale bidirectional invasions being made by other organisms that had access to the conduits.

In a recent review paper, Mazza, Buccianti, and Savorelli (2019) as‐sert that the idea of terrestrial mammals colonizing remote land‐masses by over‐water rafting is fundamentally flawed: “Grasping at straws”. A dearth of food and water, the strains imposed by fluctua‐tions in temperature and humidity, and the salty environment would make such journeys unfeasible. We here present counter arguments and re‐state the case for rafting events over range‐expansion via transitory causeways.

The view that long‐distance dispersal might explain distributions of closely related plants and animals on lands that are separated by wide expanses of sea has been around since at least the mid‐1800s. Figures such as Darlington, Darwin, Matthew, Simpson and Wallace have been enthusiastic proponents. With regards to mammals, which as a whole have a low dispersive potential over water due to their high metabolic rates and widely varied sizes and shapes, the key issue is that the successful colonizations were carried out by a restricted subset of species that travelled on vegetation mats or up‐rooted trees ('rafts'). Specifically, these are small‐bodied (low overall energy and water requirements), including some with physiological adaptations that could be beneficial during a protracted journey. As a consequence of this strong pre‐selection bias, the mammal as‐semblages that are found on the remote islands are invariably 'un‐balanced', with most source‐area components being absent. One of the most famous examples is provided by Madagascar with its

carnivorans, lemurs, rodents and tenrecs (Matthew, 1915; Simpson, 1940); the ancestors to all four lineages arrived at different times in the early and middle Cenozoic (e.g. Poux et al., 2005). The idea of land mammals rafting great distances was given further credence when in the twenty‐noughties reports of over‐water dispersed frogs were published (e.g. Measey et al., 2007; Vences et al., 2003); am‐phibians are even more physiologically challenged due to their salin‐ity intolerance.

Unsurprisingly, the number of instances of mammal LDOR is small. Figure 1 shows those cases involving passage across the open oceans (to the Canaries, Christmas Island, Enggano, Galápagos, Madagascar, Príncipe, São Tomé and South America). We purposely exclude cases from the geographically busy areas of the Caribbean, Mediterranean, most of offshore Southeast Asia and the western Pacific. Although there are numerous examples of over‐water dis‐persed mammal colonizations in these regions, the journeys were likely shorter and possibly involved ‘island‐hopping’.

To indicate the control the animals’ biologies play in the process, in Figure 2 the taxonomic order of each clade is listed. Rodentia dominate (11 of 20 events) with Eulipotyphla (true shrews) second (4). Primates (2), Carnivora (2; both are members of the typically small‐sized Viverridae) and Afrosoricida (1) com‐prise the rest. Notably, all of these orders contain heterothermic taxa (Lovegrove, 2012), and in many a scarcity of food and water induces a temporary reduction of metabolism and body tempera‐ture. For example, during Madagascar's cool dry season, small le‐murs gather in groups, often in tree holes, and undergo prolonged hibernation (such behaviour led Kappeler, 2000, to propose his “extended rafting" hypothesis to explain their colonization of the island). Other factors supporting the mechanism are records of large vegetation rafts washed into the sea, documented cases of other terrestrial vertebrates colonizing new islands using hurri‐cane‐caused rafts (Censky, Hodge, & Dudley, 1998), and evidence for reduced sea‐surface salinity due to the freshwater discharges of major rivers (Measey et al., 2007). That an ocean voyage is chal‐lenging for mammals (and amphibians) is beyond doubt; the fact that the records for transmarine dispersal in these groups is ap‐preciably rarer than in reptiles in itself lends plausibility to LDOR. Further support comes from the fact that all these mammals were small, potentially heterothermic taxa. Also, it is worth noting some of the placental clades that are not recorded: Lagomorpha, Perissodactyla and Artiodactyla, all of which are obligate homoio‐therms. Also, the artiodactyls and perissodactyls are large‐bodied.

     |  2633LETTER TO THE EDITOR

One exception to the above is hippos: prior to the arrival of hu‐mans, these artiodactyls were represented on Madagascar by three small to diminutive species: Choeropsis madagascariensis,

Hippopotamus laloumena and Hippopotamus lemerlei. We concede that even pigmy hippos may be too large to raft, and adults are un‐able to float in freshwater. However, hippos are regularly seen in

F I G U R E 1   Global map (Robinson projection) showing the islands and archipelagoes mentioned in the text. Black lettering/boxes are for a selection of landmasses and clusters where long‐distance over‐water rafting (LDOR) of mammals across open ocean is thought to have taken place (bracketed figures indicates the numbers of colonizations). For comparison, purple and green lettering/boxes denote respectively examples of colonization involving ice bridges and land bridges. Islands and archipelagoes where mammal colonization has not taken place have red lettering/boxes. Note that data from the Caribbean, Mediterranean, the western Pacific and most of offshore South‐east Asia (pale grey envelopes), are deliberately omitted —see text. The Wallace Line is indicated because the two rodent clades on Christmas Island have their nearest living relatives on the eastern side of this major biogeographical divide [Colour figure can be viewed at wileyonlinelibrary.com]

Hawaii

Príncipe [1]& São Tomé [1]

Canaries [3]

Galápagos [3]Cocos

Svalbard

Madagascar [4]

Comoros

Socotra

Seychelles

Sri Lanka

Hainan

mainlandJapan

Jeju

NewCaledonia

Mascarenes

Iceland

Falklands

Madeira

Azores

Cape Verde

St Helena

Marquesas

Society IslandsChristmas

Isl. [3]

Enggano[3]

Gt. Britain

Tasmania

Taiwan

SouthAmerica

[2]

Huxley’s “modifica�on”

Wallace’s Line

Juan FernandezIslands

Bioko

South SandwichIslands

F I G U R E 2   Data associated with the selection of islands and archipelagoes where LDOR of mammals is thought to have taken place. In the “Taxonomic information and related reproductive data” column, listed are the species/genera/clades that are present (semi‐colons separate members of different orders), plus gestation periods (days, d) and litter sizes (ls). For the last two, where data are lacking information from congenerics is presented. The † symbol indicates extinct species. For Enggano, two subspecies of Rattus rattus, R. r. diardi and R. r. vernalus, are excluded

Afr

osor

icid

a

Car

nivo

ra

Eul

ipot

yphl

a

Prim

ates

Rod

en�a

Old con�nental landsMadagascar Africa 430 1 1 1 1 Tenrecs (50–64 d; 2–32 ls), Carnivora (42–90 d; 1–6 ls), Lemurs (60–175 d; 1–3 ls) and Roden�a (24–138 d; 1–6 ls)

South America (Eocene) Africa 1,500 1 1 Caviomorphs (60–150 d; 1–13 ls) and Platyrrhines (120–225 d; 1–2 ls)

Volc. ocean-island archs./islandsacirfAseiranaC -Iberia 100 1 2 Crocidura canariensis (c . 30 d; ≥2 ls); Canariomys spp. † (N.K.) and Malpaisomys insularis † (N.K.)

htuoSsogapálaG America 930 3 Aegialomys galapagoensis (?25 d; ?3–5 ls), Megaoryzomys curioi † (N.K.) and Nesoryzomys spp. (?28 d; 2–7 ls),

512acirfAepicnírP 1 Crocidura fingui (c . 30 d; ≥2 ls)

São Tomé Africa 235 1 Crocidura thomensis (c . 30 d; ≥2 ls)

Upli�ed seamount Christmas from west of W.L. Sundaland 350 1 Crocidura trichura (c . 30 d; ≥2 ls)

Christmas from east of W.L. east of Wallace Line 1,150 2 Ra�us macleari † and Ra�us na�vita�s † (both ?20–24 d; 6–14 ls)

Upli�ed con�nental forearc521artamuSonaggnE 1 2 Paradoxurus hermaphroditus (61 d; 2–5 ls); Ra�us adustus and Ra�us enganus (both ?20–24 d; 6–14 ls)

112421slatoT

Mammal orders

Taxonomic informa�on and related reproduc�ve dataColonized land From

App. min. dist. (km)

2634  |     LETTER TO THE EDITOR

the sea and there is excellent evidence of their ability, especially of their young, to swim in saltwater and to survive being washed off coasts by storms (e.g. van der Geer, Anastasakis, & Lyras, 2015).

Despite LDOR of mammals having a high level of acceptance, Mazza et al. (2019) argue that it is unlikely to have happened be‐cause the chances of the animals surviving the passages and then being able to establish a viable colony were effectively zero. Their quantitative analysis is a much welcomed input to an otherwise often purely verbal discussion, but in some aspects it is problematic due to a confused presentation and questionable assumptions. For instance, starvation‐to‐death and dehydration‐to‐death duration data are given for a number of mammal species, but some are not relevant to the debate, for instance deer, humans and rhinoceroses. Also, with the water‐deprived examples, the two mice that survived for a month or more, Phyllotis darwini (c. 50 g) and Abrothrix olivaceus (c. 23 g), are exactly the sorts of animal the LDOR hypothesis is built around. Moreover, the idea of lack of sustenance during the journey is suspect. The potentially large uprooted trees and vegetation mats that are believed to have carried the animals might very well have harboured food. Concerning drinkable water, aside from the three rodent clades that colonized the Canaries (Figures 1 and 2), which is in a dry part of the globe (Peel, Finlayson, & McMahon, 2007), all of the other cases took place where high rainfalls occur/likely occurred on seasonal or multi‐year cycles. Additionally, Mazza et al. posit that successful colonizations were contingent upon there being moder‐ate levels of genetic variability within the founding population thus requiring the involvement of multiple species members. This, they suggest, was unlikely. However, from Figure 2 it can be seen that the gestation periods for the purported LDOR mammal groups are all 20 or more days, and litter sizes of most are relatively sizeable (those for the tenrecs are in fact the largest within the Mammalia). With a surface‐water current averaging 25 cms−1 (0.9 km h−1), c. 430 km of ocean would be covered in that time hence some of the coloniza‐tions may result from pregnant females having journeyed alone, with the newborn young plus the mother providing the initial population. Although restricted gene pools are in principle disadvantageous, marine‐island mammal populations have been shown to re‐estab‐lish rapidly sustainable genetic diversity even if founded by a single pair of individuals, probably through selection (Kaeuffer, Coltman, Chapuis, Pontier, & Réale, 2006). Moreover, rodent species, which are the most common LDOR colonizers (see above), tend to have ele‐vated levels of genetic diversity (Nabholz, Mauffrey, Bazin, Galtier, & Glemin, 2008), suggesting that they are predisposed to recover from acute population bottlenecks.

Of course if LDOR for mammals is to be rejected then land bridges are necessarily required. Concerning Mazza et al. (2019) two issues need to be addressed. The first relates to biogeographical pathways that emerged to link separated landmasses and how the terrestrial vertebrates likely responded. The second concerns our present understanding of the ocean floor and the likelihood of there being undiscovered former causeways. Mazza et al. (2019) did not consider the former, and the latter was mentioned almost as an af‐terthought in a reference to Madagascar:

….but the stratigraphic successions on the Mozambique Channel seafloor have not been ex‐plored to determine whether there is evidence for temporary emergence during this period. It is to be hoped that the relevant exploration and surveying will be conducted on the Mozambique Channel sea‐floor to reveal whether there were hitherto unde‐tected connections between Africa and Madagascar that could better explain the Malagasy fauna.

In 1940, Simpson outlined a series of 'rules' by which terrestrial mammals extended their distributions. In developing his arguments, he focused initially on the general patterns associated with range expan‐sion and contraction. He then looked at specific geographical configu‐rations. In addition to the “sweepstakes” over‐water dispersal process outlined above, Simpson considered two other situations. The first was “open corridors” using as an illustration the fauna in the southern United States between Florida and New Mexico (≥1,470 km). The ab‐sence of any appreciable occupancy barriers within the region means that the assemblages at the eastern and western ends are ostensibly the same. The second was “filter bridges” where exchange between two landmasses is partially restricted, for instance between Eurasia and North America across the Pleistocene Bering Strait, and between South America and North America via the Pliocene–Holocene Panama Isthmus. Here the climatic regime or the geographical configuration prohibits all of the species on a landmass from making the crossing. With these conduits, if a species’ range overlaps a land bridge on‐ramp, there is an excellent chance that some of its members will pass along it and establish a population on the other side. Also, transfer is bidi‐rectional. A prime illustration is provided by the land‐mammal suite on Taiwan (Figure 1). Although the island is c. 150 km from mainland Asia, the intervening seabed is <70 m deep, and would thus have been ex‐posed multiple times during the Late Pleistocene glaciations when the global sea level periodically fell 90–120 m below the present datum (Bintanja, van de Wal, & Oerlemans, 2005). Consequently, Taiwan has a rich (>30 native species) and varied fauna, including a bear Ursus thibetanus, a cat Prionailurus bengalensis, a primate Macaca cyclopis, three deer Cervus nippon, Muntiacus reevesi and Rusa unicolor, a bovid Capricornis swinhoei, a hare Lepus sinensis, and even a true mole, Mogera insularis (IUCN Red List, 2019). Presumably because of the high gene flow to/from the nearby lands, there are few endemic species; only two result from in situ cladogenesis, the rodents Niviventer coninga and Niviventer culturatus. Moreover, Taiwan hosts >40 amphibian species and a similarly large suite of reptiles. This situation, though, is not un‐common and comparable patterns are found, for example, on Bioko, Great Britain, Hainan, Jeju, Sri Lanka and Tasmania (Figure 1; Ali, 2018).

Regarding the possibility of overlooked causeways. The reality is that the floor of the global ocean, as well as that of the Mozambique Channel, is reasonably well known. Aside from academic interests, military submarines need to be able to navigate safely; communi‐cation cables need to be installed; offshore hydrocarbon resources need to be identified and evaluated. Much of this information is de‐rived from focused sonar and seismic surveys (to obtain the detail),

     |  2635LETTER TO THE EDITOR

and satellite altimetry mapping (to gain a wide coverage). For over a century we have had the evolving General Bathymetric Chart of the Oceans (e.g. GEBCO Digital Atlas, 2003), and for the last 15 years GeoMapApp (Ryan et al., 2009). The Deep Sea Drilling Project (1968–1983), Ocean Drilling Program (1984–2004), Integrated Ocean Drilling Program (2003–2013) and the International Ocean Discovery Program (2013–present) have together sampled many parts of the ocean basins, always in areas that are scientifically in‐teresting. Notably, Deep Sea Drilling Project Leg 25 cored 676 m into the sedimentary succession atop the middle sector of the Davie Ridge (Simpson et al., 1974; Figure S1). The recovered sequence spans the Upper Eocene through Quaternary; crystalline basement rocks were, though, not recovered.

Concerning the colonizations of Madagascar and the re‐lated comments by Mazza et al. (2019). Bassias (2016) posits that different sections of the Davie Ridge, which runs from just offshore southern Tanzania down the middle of the Mozambique Channel (Figure S1), were sub‐aerial at various times during the Cretaceous and Cenozoic. The evidence, based on an analysis of seismic data and dredge samples, is compelling. It should be stressed, though, that emergence was discontinuous both in time and space. The c. 600‐km‐long structure (an old transform fault that at various times has been “reworked” geologically), with its considerable relief (Ryan et al., 2009; Figure S2), should not be thought of as long promon‐tory. Telling is the title Bassias used for his manuscript and associ‐ated presentations: “Was the Mozambique Channel once scattered with islands?” If land mammals crossed from Africa to Madagascar via intervening surfaces they would still have been required to make cumulative over‐water journeys of hundreds of kilometres.

For the other islands (Christmas, Enggano, Príncipe and São Tomé), archipelagoes (Canaries and Galápagos) and continents (tropical Africa to South America in the Eocene), we contend that the chances of future surveys and drillings revealing former ter‐restrial causeways, all hundreds or even thousands of kilometres long, is negligible. Indeed, if such discoveries are made, they could well be some of the biggest findings in the histories of geology and biogeography.

In summary, although at first glance LDOR of mammals seems improbable, it needs to be placed in its proper context. First, ex‐amples of it are exceedingly rare; the overwhelming majority of land‐mammal species occupy the regions they are in because their ancestors walked there. Second, those organisms that made the ocean crossings represent a small subset of mammals with distinc‐tive physical and possibly physiological attributes. Third, rejection of the process necessarily requires causeways to explain the distribu‐tions, an unparsimonious assumption that creates additional prob‐lematic geological and biological issues. What is the evidence for these physiographical features? If they existed, then why do the bi‐ological assemblages at the ends of the various conduits not reflect the large‐scale invasions that almost certainly would have ensued?

We contend that LDOR needs to be analyzed in a wider frame‐work of entire organismal assemblages, combining evidence from fossils, timetrees, geology, physiology, palaeo‐climatology,

palaeo‐oceanography etc. Writing about “virtually zero probabili‐ties” of rafting (Mazza et al., 2019) would only make sense if based on a statistical model that accommodates all of the factors that in‐fluenced the process; hopefully this contribution will spur efforts in this potentially informative direction. Finally, as an explanation for the distribution of land‐mammals, particularly those on the remote marine islands, LDOR is not dead in water. It is in fact very much afloat and alive.

ACKNOWLEDG EMENTS

The study was in part supported by a 2018 HKU Faculty of Science EU travel award. Critiques provided by Martin Thiel and an anony‐mous reviewer helped us improve the manuscript as did Fabricio Villalobos' editorial guidance.

Jason R. Ali1

Miguel Vences2

1Department of Earth Sciences, University of Hong Kong, Hong Kong, China

2Zoological Institute, Braunschweig University of Technology, Braunschweig, Germany

CorrespondenceJason R. Ali, Department of Earth Sciences, University of Hong Kong,

Hong Kong, China.Email: jrali@hku.hk

ORCID

Jason R. Ali https://orcid.org/0000‐0002‐5214‐620X

Miguel Vences https://orcid.org/0000‐0003‐0747‐0817

R E FE R E N C E S

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Bintanja, R., van de Wal, R. S. W., & Oerlemans, J. (2005). Modelled atmo‐spheric temperatures and global sea level over the past million years. Nature, 437, 125–128.

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KEYWORDS

Caviomorphs, George Gaylord Simpson, land bridges, lemurs, long‐distance dispersal, Madagascar, mammals, platyrrhines, rodents, South America

2636  |     LETTER TO THE EDITOR

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SUPPORTING INFORMATION

Additional supporting information may be found online in the Supporting Information section at the end of the article.   

How to cite this article: Ali JR, Vences M. Mammals and long‐distance over‐water colonization: The case for rafting dispersal; the case against phantom causeways. J Biogeogr. 2019;46:2632–2636. https ://doi.org/10.1111/jbi.13659