W 2001 Dispersão BioG

Dispersal: BiogeographyDavid M Wilkinson, Liverpool John Moores University, Liverpool, UK

Dispersal is one of the fundamental processes in biogeography crucial to understanding

the distribution of organisms and important in understanding the impact of climate

change on distributions.

Introduction

Biogeography is the area of science at the interface betweenecology and geography that attempts to describe andexplain spatial patterns in the distribution of organisms. Ithas often proved much easier to describe these patternsthan to explain how they were formed. However, at themost basic level there are three fundamental processes inbiogeography: evolution, extinction and dispersal (Brownand Lomolino, 1998). Combinations of these threeprocesses explain the presence or absence of a species atany given location (Figure 1). Dispersal is therefore one ofthe key processes in biogeography and is best defined as‘the movement of organisms away from their point oforigin’ (Brown and Lomolino, 1998). The term can beapplied to individuals, species or higher taxa, so that onecan write of the dispersal of an individual seed or thedispersal (or lack of dispersal) of a whole family of plants.As well as its central role in biogeography, dispersal is ofimportance in other areas of ecology including metapopu-lation dynamics (Hanski, 1998) and population ecology,for example, as a possible mechanism for synchronizingfluctuations in local populations (Sherratt et al., 2000).

Processes of Dispersal, from Passive toActive

The most basic distinction between types of dispersal isbetween organisms that disperse using their own energy(active dispersal) and those that use energy from theenvironment (passive dispersal). Passive dispersal canmake use of energy from both the abiotic environment,such as wind and water, or energy from the bioticenvironment, an example being seed dispersal by birds.

Some organisms can use a mix of passive and activedispersal; for example, a species ofmammal could arrive onan island either by swimming or by floating on a raft ofvegetation. A range of different technical terms is appliedto different mechanisms of dispersal (Table 1), but in mostcases they fail to add any precision to discussions ofdispersal and as such are best avoided, although they havebeen widely used in the past.

Passive dispersal

Much of biodiversity ismicroscopic; for example, approxi-mately half of all phyla are composed of microscopicspecies; organisms this size can easily be dispersed by air orwater currents. This has given rise to the controversialsuggestion that microbial biodiversity is likely to be lowbecause widespread dispersal leads to limited geographicalisolation and so a low rate of speciation. There is somelimited evidence in favour of this view, mainly from workon ciliate protists (Finlay and Fenchel, 1999).Macroscopic species may also have propagules that are

small enough to be widely dispersed without requiringadaptations other than small size. Examples include manybryophyte (e.g.moss) spores; this is strikingly illustrated bysome geothermally heated volcanic soils in the Antarcticthat support bryophyte species from warmer areas ofSouth America (Smith, 1993).Larger diaspores require specific adaptations to allow

them to float in water (e.g. coconut palm, Cocos mucifera)

Article Contents

Secondary article

. Introduction

. Processes of Dispersal, from Passive to Active

. Dispersal, Migration, Vagrancy and Nomadism

. Spatial Patterns of Dispersal; Diffusion and Jump

Dispersal

. The Power of Dispersal, Examining the Tail of the

Distribution

. Centres of Dispersal or Vicariance Biogeography?

. Implications of Dispersal Limitation for Biogeography

Organism present at site

either

Evolved at the site

or

Dispersed to the site

Organism absent from site

either

Became extinct at the site

or

Was never at the site (for evolutionary and/or dispersal reasons)

Figure 1 Role of the three fundamental processes in biogeography.

1ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net

or on air currents (e.g. dandelions, Taraxacum spp.). Evenwith such adaptations, many wind-dispersed plants do notmove very far. This is illustrated by a sample (n5 25) ofwind-dispersed herbs of open habitats,which hadamedianmaximum dispersal distance of 12m (Cain et al., 1998).

An alternative adaptation for passive dispersal is tomake use of actively dispersing animals. In a study ofwaterfowl in a salt marsh in North America, over 75% ofthe birds examined had plant seeds attached to theirfeathers or feet (Vivian-Smith and Stiles, 1994). Someplants have diaspores with hooks specifically adapted fortransport on fur or feathers (e.g. cleavers,Galium aparine);however, even seeds without such adaptations can bedispersed by this method (Fischer et al., 1996).

Active dispersal

Many larger animals are capable of dispersal under theirown power. Because of their ability to fly, the greatestpotential dispersals are seen by birds and bats. Forexample, wandering albatrosses, Diomedia exulans, canmove over 8000 km from their breeding sites during thecourse of a nonbreeding year (Weimerskirch and Wilson,2000). This gives considerable potential for range expan-sion; for example, the collared dove, Streptopelia decaocto,expanded its range into Western Europe from the easternMediterranean around 1950, but the reasons for thisdramatic range expansion are unclear.

Dispersal, Migration, Vagrancy andNomadism

In addition to defining types of dispersal according tomechanisms (active or passive), a range of other terms havebeen used to describe different kinds of dispersal. Asdescribed above, dispersal can be defined as the movementof organisms away from their point of origin and can be

applied to both individuals and taxa. The term ‘migration’is often used as a synonym for dispersal (e.g. Baker, 1982;Huntley and Webb, 1989), while other workers restrict itsuse to the often annual return migrations typical of theArctic tern, Sterna paradisaea, or the monarch butterfly,Danaus plexippus. The least confusing use of these terms isprobably to consider dispersal andmigration as synonymsanduse ‘returnmigration’ for themore restricteddefinitionof migration in which the individual makes migrations inboth directions during the course of its life. Huntley andWebb (1989) argued that there are strong analogiesbetween the annual return migrations of birds and themovement of plants over a glacial/interglacial cycle, bothbeing driven by orbital forcing albeit on very different timescales. They argue that this makes migration an appro-priate term to use in both cases.Individual organisms can sometimes appear at a

location well outside their normal range. For example,birds or butterfliesmay be blown large distances by storms,or floating seeds may sometimes cross an entire ocean.Such individuals are referred to as vagrants (sometimescalled accidentals) and are of biogeographical interestbecause of the possibility that they could lead to thecolonization of a new site and so produce an increase in aspecies range. Such events, although presumably rare, arelikely to be very important in the colonization of islands.The concept of vagrant may be restricted to multicellularorganisms. If the idea that most microbes are so small thatthey can disperse anywhere is correct, then establishment,rather than dispersal, will be the key mechanism control-ling whether a population can develop at a given location.This idea is encapsulated in an old maxim of microbiology‘everything is everywhere, the environment selects’.Even when an organism is capable of active dispersal,

there are large differences in the probability of long-distance dispersal. Some organismsmove very little duringtheir life, while others cover large distances, sometimesappearing to wander at random. Such behaviour is callednomadism and the wandering albatross has been consid-ered a classic example. It has long been assumed thatduring nonbreeding periods these birds wander aimlessly,circumnavigating the southern ocean. Recent work sug-gests that this is not the case and individual birds return tofavourite nonbreeding areas (Weimerskirch and Wilson,2000). This raises the question, are other ‘nomadic’ speciesso classified because of lack of knowledge rather thanbecause they have a random dispersal pattern?

Spatial Patterns of Dispersal; Diffusionand Jump Dispersal

There are two main patterns of range expansion. Either apopulation can slowly expand from the margins of itsgeographical range (diffusion, the analogy is with a

Table 1 Technical terms often applied to the differentmechanisms of dispersal. In most cases they fail to add anyprecision to discussions of these topics; for example, ‘winddispersal’ is as precise as ‘anemochory’ and is to be preferredbecause it is likely to be understood by a wider range ofreaders. Definitions follow Van der Pijl (1969)

Endozoochory Dispersal within animals (e.g.within the gut)

Epizoochory Dispersal on the outside of animals(e.g. in fur or feathers)

Myrmechory Ant dispersalAnemochory Wind dispersalHydrochory Water dispersalAutochory Dispersal by the organism itself,

active dispersal

Dispersal: Biogeography

2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net

diffusing chemical) or a small number of individuals candisperse to a new location some distance from the currentedge of the species range (jump dispersal); or a combina-tion of these two processes can occur (Figure 2). Clearlyjump dispersal is by definition important in islandbiogeography; a classic example is given by the volcanicislands of Hawaii, which were never connected to anycontinental land mass but have a diverse flora and fauna(Carlquist, 1981). Jump dispersal is also likely to allowfaster range expansion than would be possible with purediffusion.

Some organisms are more likely to show jump dispersalthan others; for example, birds tend to be more likelycandidates than flightless (nonvolant) mammals. Manyplant species also show evidence of jump dispersal; whilefactors such as wind dispersal undoubtedly contribute tothis, several people have stressed the central role of birdstransporting seeds in plant jumpdispersal (Carlquist, 1981;Wilkinson, 1997). The implication of this is that plant jumpdispersal (and so speed of migration) would have been lessprior to the evolution of birds.

Many cases of range expansion probably involve bothdiffusion and jump dispersal. A classic example is thespread of the cattle egret, Bubulcus ibis, in the Americas.This bird, a native of Africa, colonized northeastern SouthAmerica by jump dispersal towards the end of thenineteenth century. It subsequently spread over much ofSouth America and also spread north into the southernUnited States. Maps of this spread (e.g. Brown andLomolino, 1998) suggest a pattern similar to Figure 2a.Range expansion as a steadily expanding front, albeit withsome additional jump dispersal events, such as thecolonization of many Caribbean islands. In most cases ofrange expansion the correct question is not ‘is it diffusionorjump dispersal?’ but ‘what are the relative contributions ofthese two processes?’. The big problemwith jumpdispersalis that by its nature it is a rare event and so difficult to study.

The Power of Dispersal, Examining theTail of the Distribution

Diffusion as an explanation for many range expansionsexperiences serious problems when compared to data fromQuaternary geology. As pointed out by Clement Reid atthe end of the nineteenth century, there has not beenenough time since the last glaciation for plants spreadingslowly by diffusion to return toBritain from their refugia insouthern Europe. This result was confirmed by moreformal modelling in a classic paper by Skellam (1951); theproblem is now sometimes called Reid’s Paradox (Clarket al., 1998).Most plant seeds disperse only a small distancefrom the parent plant (e.g. Cain et al., 1998), so if a statisticsuch as mean dispersal distance is used in a model of rangeexpansion then speeds much slower than those in theQuaternary fossil record are often obtained. The problemis that speed of range expansion is largely controlled by afew seeds that move much farther than the mean dispersaldistance, i.e. the extreme right hand of the distribution ofdispersal distances (Figure 3). Because such events are rare,they are very difficult to quantify. Recent modelling hasdemonstrated the great importance of these rare extremedispersal events in determining the rate of migration of apopulation such as oak, Quercus sp., in Europe at the endof the last glaciation (Clark et al., 1998). Both Reid andSkellan implicated birds in these rapid plant migrationevents, but for a full understanding more data is requiredon these rare jump dispersal events.

Centres of Dispersal or VicarianceBiogeography?

The reliance of dispersal biogeography on chance eventshas been seen as undesirable by some biologists as theyview the resulting explanations as untestable ‘just so

(a) (b) (c)

Figure 2 Types of range expansion. (a) Diffusion. Range expansion as a steady expanding front. (b) Jump dispersal. Founding a new population welloutside the species current range. (c) Combination of diffusion and jump dispersal. Over time the new population founded by a jump dispersal event maymerge with the main population as both expand by diffusion.



stories’. Vicariance biogeography attempted to addressthis problem by downplaying the importance of dispersaland replacing it with the idea that a taxon’s range can bedivided by the formationof physical barriers. For example,if closely related taxa are found on both sides on an ocean,dispersal biogeography would point to a dispersal event asthe explanation (as in the cattle egret example), whilevicariance biogeographers would suggest that a formerlycontinuous distribution of an ancestral taxon had beendivided by the formation of the ocean. The advantage inthe vicariant position is that the physical division of thetaxon’s range is open to independent geological verifica-tion. These different traditions can be traced back to thenineteenth century when Charles Darwin emphasizeddispersal and the importance of ‘occasional means ofdistribution’, while his close friend Joseph Dalton Hookeremphasized the physical dissection of previously contin-uous distributions.Wilson (1991) tabulated the differencesbetween dispersal (migration) biogeography and vicar-iance, along with the closely related ideas of panbiogeo-graphy, in detail. The problems with the vicarianceapproach include the assumption that all speciation isdue to geographical isolation (the alternative, sympatricspeciation, is increasingly the subject of much activeresearch) and the refusal to consider long-distancedispersal, despite themany cases described in the literature.Most modern biogeographers work within the Darwiniandispersal traditionwhile allowing that vicariant events (e.g.due to plate tectonics) can sometimes be important. Thecentral paradigm of dispersal biogeography is that taxausually originate at a single location (a centre of dispersal)and may then expand their range to produce their presentdistribution (Wilson, 1991).

Implications of Dispersal Limitation forBiogeography

It is a common observation that different species are foundin different parts of the world. One explanation for this isthat species are found where the environmental conditionsare suitable for them. This could be true for many free-living microbes, which are small enough to easily disperse.However for many larger organisms it is clear that thedistribution of suitable habitats is not the only factorlimiting their distribution. This is demonstrated by theexample of the cattle egret, which after managing to crossthe Atlantic colonized large areas of the Americas. Clearlysuitable habitat was available in America; the limitingfactor was dispersal from Africa. The same point isunderlined by the success of many species that have beenintroduced to Britain and survived to produce self-sustaining populations; these include birds such as theCanada goose,Branta canadensis, and ruddyduck,Oxyurajamaicensis, as well as mammals such as the brown rat,Rattus norvegicus. When humans solved these animals’dispersal problems theywere able to expand their ranges toinclude Britain. Humans now play a major role in thedispersal of many organisms; for example, they haveintroduced over 1000 plant species to the British country-side, of which around 70 have been widely naturalized(Crawley, 1997).

Past dispersal limitation

The idea of movement out from a centre of dispersal isnicely illustrated by our own species, Homo sapiens. Itappears to have originated in Africa in excess of 100 000 yrago; by approximately 50 000 yr ago, theywere in Asia andevenAustralia and arrived in theAmericas some time later,although the exact time is still controversial. However,remote islands such as Hawaii and Easter Island were notreached until around AD 500 because of dispersalproblems.In the case of humans on Hawaii, it appears that the

difficulties in dispersal, rather than environmental condi-tions on the island, were the rate-determine step in thecolonization process. But this is not always the case andmigration rates can be constrained by environmentalfactors such as rate of climate change, rather than by thepotential dispersal rate. Consider the migration rate ofEuropean trees after the end of the last glaciation (Table 2):the speeds reconstructed from analysis of fossil pollenpreserved in peat and lake sediments rule out diffusion(Reid’s paradox discussed above), andmodelling by Clark(1998) suggests that these migration velocities may nothave reached their maximum, ‘being stalled by rates ofclimate change, geography or both’. This has implicationsfor future migration rates in response to climate change(discussed below).

Dispersal distance

Freq

uenc

y

Figure 3 Distributionof seed dispersal distances for many organisms has avery long tail with a few diaspores or individuals dispersing much furtherthan the average distance. The shape of the curve illustrated is typical forplant species as different as the herb Asarum canadense and the tree Piceasp.



On a larger geological time scale, a major constraint ondispersal has been the changing patterns of the continentsdue to plate tectonics. For example, the formation of theHimalayas as a result of collisions between continentalplates isolated many species on either side of the barrier,while creating a habitat for others such as the cold-adaptedsnow leopard, Panthera uncia.

Future dispersal limitations

There is now great concern over climate change caused byfactors such as the increase in greenhouse gases. One of themain insights from the study of past dispersal events is thatmost species have responded to past climatic changes bymigration rather than by in situ adaptation to the newconditions (Huntley, 1994). Thus a key question is whetherorganisms will be able to disperse at a speed that will allowthem to track the changing climate.

The fact that immobile organisms, such as plants, canmigrate at rates well in excess of those predicted from theiraverage dispersal distance could hold promise for popula-tions in the face of future global changes (Clark, 1998).However, the future changes are unlikely to be identical tothose in the past. For example, it is possible that the rate ofclimate change could be greater than any seen in the last 2.4million yr (Huntley, 1994). In addition, the nature of thelandscape through which organisms disperse has nowchanged through agriculture and urban development. It isclearly vital to preserve the countryside in a state thatallows organisms to migrate through it unimpeded inresponse to climate change. This may no longer be the casein many parts of the world, so that the optimism based onpast migration rates may be misplaced. Modelling studiesby Dyer (1995) have illustrated the way different speciesmay showvariations in rates of response to climate change.In his model the fastest migration rate observed for wind-dispersed plants was over 1.5 times slower than that forbird-dispersed species. However, Wilkinson (1997) hasargued that, at the temporal and spatial scales of interest inbiogeography, such simple classifications of dispersal types(as listed in Table 1) can break down, so that, for example,wind-dispersed seeds can be dispersed by birds.

Human influence has had another effect on dispersal,namely reducing the effects of dispersal barriers bymoving

organisms around the world. A historical example of thiseffect is the Polynesian colonization of Henderson Island,in the Pitcairn groupof islands in the SouthPacific.At leastthree species of snails first appear in the Polynesianoccupation horizons. At the same time at least five nativesnail species became extinct, probably through habitatdestruction caused by humans, although competition withthe introduced snails cannot be ruled out (Preece, 1998). Astudy of the current British flora by Hodkinson andThompson (1997) found that many species were nowdispersed by soil carried bymotor cars, or as topsoil and byother human-based dispersal mechanisms. In the marineenvironment, transport on the hulls of ships is now amajordispersal mechanism for some types of bryozoa (Wattset al., 1998). When a species is dispersed to another part ofthe world by human actions, its main parasites andpredators can be left behind; occasionally this can causea dramatic increase in its population at the new site and theintroduced organism can become a pest species. Adramatic illustration of the effects of such a release fromnatural enemies is rubber,Hevea brasiliensis, which cannotbe grown as a plantation crop in its native Brazil but is amajor plantation crop in South East Asia where it has beenintroduced without many of the species that feed on it inSouth America (Crawley, 1997). If an introduced speciesbecomes a major problem, one possibility is to introducesome of its natural enemies. This was done to control thecactus Opuntia ficus-indica, introduced to South Africafrom the Americas. which at one point infested 900 000 haof South Africa (Nobel, 1994). Increasingly, humanactions are reducing the effect of barriers to dispersal; thiscan confront species of restricted range with new compe-titors that are often widespread successful species (such asOpuntia) that can outcompete them, leading to a decline ofbiodiversity.

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Table 2 Maximum rate of migration of some European treetaxa during the past 10 000 yr

TaxaMaximum migration rate(m per yr)

Hazel, Corylus 1500Beech, Fagus 300Ash, Fraxinus 500Oak, Quercus 500Lime, Tilia 500Elm, Ulmus 1000



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Baker RR (1978) The Evolutionary Ecology of Animal Migration.

London: Hodder and Stoughton.

Cox CB and Moore PD (2000) Biogeography, 6th edn. Oxford:

Blackwell.

Pitelka LF, Garden RH, Ash J et al. (1997) Plant migration and climate

change. American Scientist 85: 464–473.

Thornton I (1996) Krakatau. Cambridge, MA: Harvard University

Press.

Whittaker RJ (1998) Island Biogeography. Oxford: Oxford University

Press.

Wilkinson DM (1999) Plants on the move. New Scientist 2178(suppl.):

S1–S4.



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