Dispersal: Biogeography

David 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.

Secondary article
Article Contents
. 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?

Introduction
Biogeography is the area of science at the interface between ecology and geography that attempts to describe and explain spatial patterns in the distribution of organisms. It has often proved much easier to describe these patterns than to explain how they were formed. However, at the most basic level there are three fundamental processes in biogeography: evolution, extinction and dispersal (Brown and Lomolino, 1998). Combinations of these three processes explain the presence or absence of a species at any given location (Figure 1). Dispersal is therefore one of the key processes in biogeography and is best dened as the movement of organisms away from their point of origin (Brown and Lomolino, 1998). The term can be applied to individuals, species or higher taxa, so that one can write of the dispersal of an individual seed or the dispersal (or lack of dispersal) of a whole family of plants. As well as its central role in biogeography, dispersal is of importance in other areas of ecology including metapopulation dynamics (Hanski, 1998) and population ecology, for example, as a possible mechanism for synchronizing uctuations in local populations (Sherratt et al., 2000).

. Implications of Dispersal Limitation for Biogeography

Some organisms can use a mix of passive and active dispersal; for example, a species of mammal could arrive on an island either by swimming or by oating on a raft of vegetation. A range of dierent technical terms is applied to dierent mechanisms of dispersal (Table 1), but in most cases they fail to add any precision to discussions of dispersal and as such are best avoided, although they have been widely used in the past.

Passive dispersal
Much of biodiversity is microscopic; for example, approximately half of all phyla are composed of microscopic species; organisms this size can easily be dispersed by air or water currents. This has given rise to the controversial suggestion that microbial biodiversity is likely to be low because widespread dispersal leads to limited geographical isolation and so a low rate of speciation. There is some limited evidence in favour of this view, mainly from work on ciliate protists (Finlay and Fenchel, 1999). Macroscopic species may also have propagules that are small enough to be widely dispersed without requiring adaptations other than small size. Examples include many bryophyte (e.g. moss) spores; this is strikingly illustrated by some geothermally heated volcanic soils in the Antarctic that support bryophyte species from warmer areas of South America (Smith, 1993). Larger diaspores require specic adaptations to allow them to oat in water (e.g. coconut palm, Cocos mucifera)

Processes of Dispersal, from Passive to Active

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

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.

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Table 1 Technical terms often applied to the dierent mechanisms of dispersal. In most cases they fail to add any precision to discussions of these topics; for example, wind dispersal is as precise as anemochory and is to be preferred because it is likely to be understood by a wider range of readers. Denitions follow Van der Pijl (1969) Endozoochory Epizoochory Myrmechory Anemochory Hydrochory Autochory Dispersal within animals (e.g. within the gut) Dispersal on the outside of animals (e.g. in fur or feathers) Ant dispersal Wind dispersal Water dispersal Dispersal by the organism itself, active dispersal

or on air currents (e.g. dandelions, Taraxacum spp.). Even with such adaptations, many wind-dispersed plants do not move very far. This is illustrated by a sample (n 5 25) of wind-dispersed herbs of open habitats, which had a median maximum dispersal distance of 12 m (Cain et al., 1998). An alternative adaptation for passive dispersal is to make use of actively dispersing animals. In a study of waterfowl in a salt marsh in North America, over 75% of the birds examined had plant seeds attached to their feathers or feet (Vivian-Smith and Stiles, 1994). Some plants have diaspores with hooks specically adapted for transport on fur or feathers (e.g. cleavers, Galium aparine); however, even seeds without such adaptations can be dispersed by this method (Fischer et al., 1996).

Active dispersal
Many larger animals are capable of dispersal under their own power. Because of their ability to y, the greatest potential dispersals are seen by birds and bats. For example, wandering albatrosses, Diomedia exulans, can move over 8000 km from their breeding sites during the course of a nonbreeding year (Weimerskirch and Wilson, 2000). This gives considerable potential for range expansion; for example, the collared dove, Streptopelia decaocto, expanded its range into Western Europe from the eastern Mediterranean around 1950, but the reasons for this dramatic range expansion are unclear.

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 its use to the often annual return migrations typical of the Arctic tern, Sterna paradisaea, or the monarch buttery, Danaus plexippus. The least confusing use of these terms is probably to consider dispersal and migration as synonyms and use return migration for the more restricted denition of migration in which the individual makes migrations in both directions during the course of its life. Huntley and Webb (1989) argued that there are strong analogies between the annual return migrations of birds and the movement of plants over a glacial/interglacial cycle, both being driven by orbital forcing albeit on very dierent time scales. They argue that this makes migration an appropriate term to use in both cases. Individual organisms can sometimes appear at a location well outside their normal range. For example, birds or butteries may be blown large distances by storms, or oating seeds may sometimes cross an entire ocean. Such individuals are referred to as vagrants (sometimes called accidentals) and are of biogeographical interest because of the possibility that they could lead to the colonization of a new site and so produce an increase in a species range. Such events, although presumably rare, are likely to be very important in the colonization of islands. The concept of vagrant may be restricted to multicellular organisms. If the idea that most microbes are so small that they can disperse anywhere is correct, then establishment, rather than dispersal, will be the key mechanism controlling 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 dierences in the probability of longdistance dispersal. Some organisms move very little during their life, while others cover large distances, sometimes appearing to wander at random. Such behaviour is called nomadism and the wandering albatross has been considered a classic example. It has long been assumed that during nonbreeding periods these birds wander aimlessly, circumnavigating the southern ocean. Recent work suggests that this is not the case and individual birds return to favourite nonbreeding areas (Weimerskirch and Wilson, 2000). This raises the question, are other nomadic species so classied because of lack of knowledge rather than because they have a random dispersal pattern?

Dispersal, Migration, Vagrancy and Nomadism

In addition to dening types of dispersal according to mechanisms (active or passive), a range of other terms have been used to describe dierent kinds of dispersal. As described above, dispersal can be dened as the movement of organisms away from their point of origin and can be
2

Spatial Patterns of Dispersal; Diffusion and Jump Dispersal

There are two main patterns of range expansion. Either a population can slowly expand from the margins of its geographical range (diusion, the analogy is with a

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Dispersal: Biogeography

diusing chemical) or a small number of individuals can disperse to a new location some distance from the current edge of the species range (jump dispersal); or a combination of these two processes can occur (Figure 2). Clearly jump dispersal is by denition important in island biogeography; a classic example is given by the volcanic islands of Hawaii, which were never connected to any continental land mass but have a diverse ora and fauna (Carlquist, 1981). Jump dispersal is also likely to allow faster range expansion than would be possible with pure diusion. Some organisms are more likely to show jump dispersal than others; for example, birds tend to be more likely candidates than ightless (nonvolant) mammals. Many plant species also show evidence of jump dispersal; while factors such as wind dispersal undoubtedly contribute to this, several people have stressed the central role of birds transporting seeds in plant jump dispersal (Carlquist, 1981; Wilkinson, 1997). The implication of this is that plant jump dispersal (and so speed of migration) would have been less prior to the evolution of birds. Many cases of range expansion probably involve both diusion and jump dispersal. A classic example is the spread of the cattle egret, Bubulcus ibis, in the Americas. This bird, a native of Africa, colonized northeastern South America by jump dispersal towards the end of the nineteenth century. It subsequently spread over much of South America and also spread north into the southern United States. Maps of this spread (e.g. Brown and Lomolino, 1998) suggest a pattern similar to Figure 2a. Range expansion as a steadily expanding front, albeit with some additional jump dispersal events, such as the colonization of many Caribbean islands. In most cases of range expansion the correct question is not is it diusion or jump dispersal? but what are the relative contributions of these two processes?. The big problem with jump dispersal is that by its nature it is a rare event and so dicult to study.

The Power of Dispersal, Examining the Tail of the Distribution

Diusion as an explanation for many range expansions experiences serious problems when compared to data from Quaternary geology. As pointed out by Clement Reid at the end of the nineteenth century, there has not been enough time since the last glaciation for plants spreading slowly by diusion to return to Britain from their refugia in southern Europe. This result was conrmed by more formal modelling in a classic paper by Skellam (1951); the problem is now sometimes called Reids Paradox (Clark et al., 1998). Most plant seeds disperse only a small distance from the parent plant (e.g. Cain et al., 1998), so if a statistic such as mean dispersal distance is used in a model of range expansion then speeds much slower than those in the Quaternary fossil record are often obtained. The problem is that speed of range expansion is largely controlled by a few seeds that move much farther than the mean dispersal distance, i.e. the extreme right hand of the distribution of dispersal distances (Figure 3). Because such events are rare, they are very dicult to quantify. Recent modelling has demonstrated the great importance of these rare extreme dispersal events in determining the rate of migration of a population such as oak, Quercus sp., in Europe at the end of the last glaciation (Clark et al., 1998). Both Reid and Skellan implicated birds in these rapid plant migration events, but for a full understanding more data is required on these rare jump dispersal events.

Centres of Dispersal or Vicariance Biogeography?

The reliance of dispersal biogeography on chance events has been seen as undesirable by some biologists as they view 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 well outside the species current range. (c) Combination of diffusion and jump dispersal. Over time the new population founded by a jump dispersal event may merge with the main population as both expand by diffusion.

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Dispersal: Biogeography

Implications of Dispersal Limitation for Biogeography

It is a common observation that dierent species are found in dierent parts of the world. One explanation for this is that species are found where the environmental conditions are suitable for them. This could be true for many freeliving microbes, which are small enough to easily disperse. However for many larger organisms it is clear that the distribution of suitable habitats is not the only factor limiting their distribution. This is demonstrated by the example of the cattle egret, which after managing to cross the Atlantic colonized large areas of the Americas. Clearly suitable habitat was available in America; the limiting factor was dispersal from Africa. The same point is underlined by the success of many species that have been introduced to Britain and survived to produce selfsustaining populations; these include birds such as the Canada goose, Branta canadensis, and ruddy duck, Oxyura jamaicensis, as well as mammals such as the brown rat, Rattus norvegicus. When humans solved these animals dispersal problems they were able to expand their ranges to include Britain. Humans now play a major role in the dispersal of many organisms; for example, they have introduced over 1000 plant species to the British countryside, of which around 70 have been widely naturalized (Crawley, 1997).
Frequency

Dispersal distance

Figure 3 Distribution of seed dispersal distances for many organisms has a very long tail with a few diaspores or individuals dispersing much further than the average distance. The shape of the curve illustrated is typical for plant species as different as the herb Asarum canadense and the tree Picea sp.

stories. Vicariance biogeography attempted to address this problem by downplaying the importance of dispersal and replacing it with the idea that a taxons range can be divided by the formation of physical barriers. For example, if closely related taxa are found on both sides on an ocean, dispersal biogeography would point to a dispersal event as the explanation (as in the cattle egret example), while vicariance biogeographers would suggest that a formerly continuous distribution of an ancestral taxon had been divided by the formation of the ocean. The advantage in the vicariant position is that the physical division of the taxons range is open to independent geological verication. These dierent traditions can be traced back to the nineteenth century when Charles Darwin emphasized dispersal and the importance of occasional means of distribution, while his close friend Joseph Dalton Hooker emphasized the physical dissection of previously continuous distributions. Wilson (1991) tabulated the dierences between dispersal (migration) biogeography and vicariance, along with the closely related ideas of panbiogeography, in detail. The problems with the vicariance approach include the assumption that all speciation is due to geographical isolation (the alternative, sympatric speciation, is increasingly the subject of much active research) and the refusal to consider long-distance dispersal, despite the many cases described in the literature. Most modern biogeographers work within the Darwinian dispersal tradition while allowing that vicariant events (e.g. due to plate tectonics) can sometimes be important. The central paradigm of dispersal biogeography is that taxa usually originate at a single location (a centre of dispersal) and may then expand their range to produce their present distribution (Wilson, 1991).

Past dispersal limitation

The idea of movement out from a centre of dispersal is nicely illustrated by our own species, Homo sapiens. It appears to have originated in Africa in excess of 100 000 yr ago; by approximately 50 000 yr ago, they were in Asia and even Australia and arrived in the Americas some time later, although the exact time is still controversial. However, remote islands such as Hawaii and Easter Island were not reached until around AD 500 because of dispersal problems. In the case of humans on Hawaii, it appears that the diculties in dispersal, rather than environmental conditions on the island, were the rate-determine step in the colonization process. But this is not always the case and migration rates can be constrained by environmental factors such as rate of climate change, rather than by the potential dispersal rate. Consider the migration rate of European trees after the end of the last glaciation (Table 2): the speeds reconstructed from analysis of fossil pollen preserved in peat and lake sediments rule out diusion (Reids paradox discussed above), and modelling by Clark (1998) suggests that these migration velocities may not have reached their maximum, being stalled by rates of climate change, geography or both. This has implications for future migration rates in response to climate change (discussed below).

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Table 2 Maximum rate of migration of some European tree taxa during the past 10 000 yr Taxa Hazel, Corylus Beech, Fagus Ash, Fraxinus Oak, Quercus Lime, Tilia Elm, Ulmus Maximum migration rate (m per yr) 1500 300 500 500 500 1000

On a larger geological time scale, a major constraint on dispersal has been the changing patterns of the continents due to plate tectonics. For example, the formation of the Himalayas as a result of collisions between continental plates isolated many species on either side of the barrier, while creating a habitat for others such as the cold-adapted snow leopard, Panthera uncia.

Future dispersal limitations

There is now great concern over climate change caused by factors such as the increase in greenhouse gases. One of the main insights from the study of past dispersal events is that most species have responded to past climatic changes by migration rather than by in situ adaptation to the new conditions (Huntley, 1994). Thus a key question is whether organisms will be able to disperse at a speed that will allow them to track the changing climate. The fact that immobile organisms, such as plants, can migrate at rates well in excess of those predicted from their average dispersal distance could hold promise for populations in the face of future global changes (Clark, 1998). However, the future changes are unlikely to be identical to those in the past. For example, it is possible that the rate of climate change could be greater than any seen in the last 2.4 million yr (Huntley, 1994). In addition, the nature of the landscape through which organisms disperse has now changed through agriculture and urban development. It is clearly vital to preserve the countryside in a state that allows organisms to migrate through it unimpeded in response to climate change. This may no longer be the case in many parts of the world, so that the optimism based on past migration rates may be misplaced. Modelling studies by Dyer (1995) have illustrated the way dierent species may show variations in rates of response to climate change. In his model the fastest migration rate observed for winddispersed plants was over 1.5 times slower than that for bird-dispersed species. However, Wilkinson (1997) has argued that, at the temporal and spatial scales of interest in biogeography, such simple classications of dispersal types (as listed in Table 1) can break down, so that, for example, wind-dispersed seeds can be dispersed by birds. Human inuence has had another eect on dispersal, namely reducing the eects of dispersal barriers by moving

organisms around the world. A historical example of this eect is the Polynesian colonization of Henderson Island, in the Pitcairn group of islands in the South Pacic. At least three species of snails rst appear in the Polynesian occupation horizons. At the same time at least ve native snail species became extinct, probably through habitat destruction caused by humans, although competition with the introduced snails cannot be ruled out (Preece, 1998). A study of the current British ora by Hodkinson and Thompson (1997) found that many species were now dispersed by soil carried by motor cars, or as topsoil and by other human-based dispersal mechanisms. In the marine environment, transport on the hulls of ships is now a major dispersal mechanism for some types of bryozoa (Watts et al., 1998). When a species is dispersed to another part of the world by human actions, its main parasites and predators can be left behind; occasionally this can cause a dramatic increase in its population at the new site and the introduced organism can become a pest species. A dramatic illustration of the eects of such a release from natural enemies is rubber, Hevea brasiliensis, which cannot be grown as a plantation crop in its native Brazil but is a major plantation crop in South East Asia where it has been introduced without many of the species that feed on it in South America (Crawley, 1997). If an introduced species becomes a major problem, one possibility is to introduce some of its natural enemies. This was done to control the cactus Opuntia cus-indica, introduced to South Africa from the Americas. which at one point infested 900 000 ha of South Africa (Nobel, 1994). Increasingly, human actions are reducing the eect of barriers to dispersal; this can confront species of restricted range with new competitors that are often widespread successful species (such as Opuntia) that can outcompete them, leading to a decline of biodiversity.

References
Baker RR (1982) Migration, Paths Through Time and Space. London: Hodder and Stoughton. Brown JH and Lomolino MV (1998) Biogeography. Sunderland, MA: Sinauer. Cain ML, Damman H and Muir A (1998) Seed dispersal and the Holocene migration of woodland herbs. Ecological Monographs 68: 325347. Carlquist S (1981) Chance dispersal. American Scientist 69: 509516. Clark JS (1998) Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. American Naturalist 152: 204 224. Clark JS, Fastie C, Hurtt G C et al. (1998) Reids paradox of rapid plant migration. Bioscience 48: 1324. Crawley MJ (1997) Plant Ecology, (chap. 19). Oxford: Blackwell. Dyer JM (1995) Assessment of climatic warming using a model of forest species migration. Ecological Modelling 79: 199219. Finlay BJ and Fenchel T (1999) Divergent perspectives on protist species richness. Protist 150: 229233. Fischer SF, Poschlod P and Beinlich B (1996) Experimental studies on the dispersal of plants and animals on sheep in calcareous grassland. Journal of Applied Ecology 33: 12061222.

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Hanski I (1998) Metapopulation dynamics. Nature 396: 4149. Hodkinson DJ and Thompson K (1997) Plant dispersal: the role of man. Journal of Applied Ecology 34: 14841496. Huntley B (1994) Plant species response to climate change: implications for the conservation of European birds. Ibis 137: s127s138. Huntley B and Birks HJB (1983) An Atlas of Past and Present Pollen Maps for Europe 0 13000 BP. Cambridge, UK: Cambridge University Press. Huntley B and Webb T (1989) Migration: species response to climatic variations caused by changes in the Earths orbit. Journal of Biogeography 16: 519. Nobel PS (1994) Remarkable Agaves and Cacti. Oxford: Oxford University Press. Preece RC (1998) Impact of early Polynesian occupation on the land snail fauna of Henderson Island, Pitcairn Group (South Pacic). Philosophical Transactions of the Royal Society of London B 353: 347 368. Sherratt TN, Lambin X, Petty SJ et al. (2000) Use of coupled oscillator models to understand synchrony and travelling waves in populations of the Field Vole Microtus agrestis in Northern England. Journal of Applied Ecology 37(supplement 1): 148158. Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38: 196218. Smith RIL (1993) The role of bryophyte propagule banks in primary succession: case study of an Antarctic fellfeild soil. In: Miles J and Walton DWH (eds) Primary Succession on Land. Oxford: Blackwell. Van der Pijl L (1969) Principles of Dispersal in Higher Plants. Berlin: Springer-Verlag. Vivian-Smith G and Stiles EW (1994) Dispersal of salt marsh seeds on the feet and feathers of waterfowl. Wetlands 14: 316319.

Watts PC, Thorpe JP and Taylor PD (1998) Natural and anthropogenic dispersal mechanisms in the marine environment a study using cheilostome bryozoa. Philosophical Transactions of the Royal Society of London B 353: 453464. Weimerskirch H and Wilson RP (2000) Oceanic respite for wandering albatrosses. Nature 406: 955956. Wilkinson DM (1997) Plant colonization: are wind dispersed seeds really dispersed by birds at larger spatial and temporal scales? Journal of Biogeography 24: 6165. Wilson JB (1991) A comparison of biogeographic models: migration, vicariance and panbiogeography. Global Ecology and Biogeography Letters 1: 8487.

Further Reading
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: 464473. 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.): S1S4.

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