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Introduction

  1. Top of page
  2. Introduction
  3. The Freckleton & Watkinson typology
  4. The importance of regional processes
  5. Is the metapopulation concept still useful for plants?
  6. Acknowledgements
  7. References

Metapopulation theory (summarized by Hanski 1999) is one of the most influential developments in ecology of recent decades, for example as a cornerstone of conservation biology, and as a theoretical basis for studies of dispersal and of the distribution and abundance of species. A synthesis of metapopulation theory and landscape ecology has been regarded as a key to analyses of the ecological consequences of ongoing landscape changes (Wiens 1997). Although successfully applied to many regional systems of animal populations, the usefulness of metapopulation theory for studies of plants is still open to debate. As Husband & Barrett (1996) and Eriksson (1996) concluded, rather few studies have documented metapopulations in plants, and the same holds for other forms of regional dynamics, e.g. source-sink populations and remnant populations. In a recent paper, Freckleton & Watkinson (2002) have critically reviewed studies of plant metapopulations, with the objectives of assessing whether regional populations of plants really are metapopulations, and suggesting a new typology for different forms of plant regional dynamics. Freckleton & Watkinson stress, and we agree, that these issues are not merely semantic. The concepts of regional dynamics not only determine the ways in which empirical studies are performed, but also influence the interpretation of data (illustrated by Freckleton & Watkinson with studies claiming, but not showing, the existence of metapopulations) and the modelling of spatial dynamics of plant populations.

Freckleton & Watkinson (2002) begin by listing four criteria that must be fulfilled in order to regard a regional population as a metapopulation: (i) suitable habitat occurs as discrete patches that may be occupied or unoccupied; (ii) all local populations have a measurable extinction risk; (iii) habitat patches are interconnected by dispersal, allowing the possibility of re-colonization; and (iv) local populations are not completely synchronized in their dynamics. If these criteria are met, regional dynamics cannot be inferred from local processes, and local dynamics cannot be understood without referring to regional patterns or processes.

Freckleton & Watkinson (2002) conclude that, given these criteria, very few cases exist where plant metapopulations have been documented. Indeed, there are a number of reasons why plants may not develop metapopulations in the same way as short-lived mobile animals. The existence of long-lived life cycle stages (e.g. seeds or vegetative ramets) means that a local population may persist for a long time even though the patch has become unsuitable. Successful dispersal and recruitment may be very sporadic, and therefore re-colonization is unlikely after local population extinction. Dispersal over long distances may be governed by chance events. The definition of ‘long distance’ may differ between species, but in many cases it may be no more than a few hundred metres (Cain et al. 2000). Suitable habitat is difficult to define, and suitability is likely to be a continuous function of abiotic and biotic environmental factors. Freckleton & Watkinson propose that, using a metapopulation concept for describing regional populations, many plant regional populations would be described as non-equilibrium metapopulations, a conclusion we also reached for plants in fragmented habitats (Eriksson & Ehrlén 2001).

We agree with Freckleton & Watkinson (2002) that it is difficult to assess whether plants in general fulfil the criteria for metapopulations. However, we disagree with their suggestions on a new typology for regional dynamics. We also believe that their conclusions concerning the difficulties in documenting metapopulations in plants may be interpreted as indicating that local processes are sufficient for understanding regional patterns of plant populations, although we acknowledge that this may not have been their intention.

We have three objectives here: (i) to comment on the typology of regional dynamics suggested by Freckleton & Watkinson (2002); (ii) to suggest how regional processes might be of importance to plant distributions irrespective of whether plants have metapopulations; and (iii) to argue that metapopulation theory should be developed further as a tool for studies of plants, rather than being replaced by other concepts.

The Freckleton & Watkinson typology

  1. Top of page
  2. Introduction
  3. The Freckleton & Watkinson typology
  4. The importance of regional processes
  5. Is the metapopulation concept still useful for plants?
  6. Acknowledgements
  7. References

Freckleton & Watkinson (2002) suggest that regional plant populations may take three main forms: ‘metapopulations’, ‘regional ensembles’ and ‘spatially extended populations’. These three forms basically depend on the proportion of suitable habitat in the region. If suitable habitats (S) cover a much larger area than unsuitable habitats (U), i.e. S >> U, plants develop ‘spatially extended populations’. If U covers a much larger area than S, i.e. U >> S, plants develop regional ensembles where isolation effectively prevents migration between patches of suitable habitat, and recolonizations do not occur after local extinctions. Metapopulations are argued to occur at intermediate levels of S and U, i.e. where the proportion of suitable habitat is such that plants occur in isolated patches but these patches are close enough to allow for colonizations. The suggested link between S and U and the type of regional dynamics is that the relationship between local birth and death processes (B and D) and regional immigration and emigration rates (I and E) in effect determines the type of regional dynamics displayed. However, it is important to realize that, whereas the relative size of I and E vs. B and D describes the dynamics within population units (Thomas & Kunin 1999), variation in any or all of I, E, B and D may be crucial for regional dynamics. For example, it is the variation in immigration rates with distance that underlies correlations between patch occupancy and patch isolation predicted by metapopulation models. Even very rare colonization events may be decisive for the dynamics of a regional population. We can therefore not say anything about the likelihood of colonization of ‘empty’ patches, nor about whether colonization reflects habitat configuration (which is a feature of metapopulations), just by assessing the relationship between B + D and I + E.

The argument that metapopulations are rare among plants may then boil down to the fact that relatively few species are intermediate with respect to both the proportion of habitat that is suitable and their migration rate. We suggest that what is considered as ‘intermediate’, and hence metapopulation dynamics, is largely a matter of spatial and temporal scale. For example, Freckleton & Watkinson (2002, p. 420) define ‘region’ as a ‘large area that encompasses a set of local populations’. As most plants are patchily distributed at some spatial scale, there will always be a possibility that a study, arbitrarily delimited, will find S > U, U > S or U >> S, simply as a result of the chosen spatial scale. What may be regarded at one scale as a ‘spatially extended population’ (SEP), according to the Freckleton & Watkinson typology, may be regarded as a metapopulation or as a ‘regional ensemble’ at larger spatial scales. Unless there is some absolute scale by which we can define a region, the prediction that a relationship between S and U determines the form of regional dynamics becomes very difficult to examine.

The temporal scale of studies will also be crucial for the type of regional dynamics observed. Colonization rates so low that they are difficult to record in studies spanning over years or decades, may still result in regional dynamics that depend on habitat configuration. Several recent studies have convincingly shown that dispersal over long distances (or ‘plant migration’) cannot be predicted by the use of ordinary dispersal curves (Cain et al. 1998; Clark 1998; Clark et al. 1998; Higgins & Richardson 1999; Bullock et al. 2002). Over a certain distance, chance events will have a dominating influence over the dispersal process. Such chance events are indeed very difficult to document, but they must be included in any model of dispersal in plants. Several studies have shown that the proportion of suitable habitat patches that are occupied depends on patch isolation at a landscape scale (km2), even for species where colonizations and extinctions are not observed (Quintana-Ascencio & Menges 1996; Bastin & Thomas 1999; Dupré & Ehrlén 2002).

Several authors have acknowledged the crucial importance of scale in studies of regional dynamics (e.g. Whittaker & Levin 1977; Thomas & Kunin 1999). Any attempt to assign plant populations to a specific regional type that does not make reference to a specific spatial and temporal scale is therefore bound to be problematic. We feel that the solution to much of the problem lies in abandoning attempts to assign every population or network into a defined category. Instead we should focus on the processes and ask whether our understanding of a particular study system can be derived from a simple extrapolation of the processes acting within populations or whether we may gain something from the explicit consideration of factors operating at larger spatial scales.

We agree with Thomas & Kunin (1999, p. 655), who argued that ‘category-based schemes encourage unnecessary and unproductive dispute: two authors could examine a single data set, and yet reach different conclusions as to whether it represents a metapopulation or a patchy population’. The case with Vulpia ciliata used as an example of a ‘regional ensemble’ by Freckleton & Watkinson (2002, p. 430) may illustrate this problem. Freckleton & Watkinson give four reasons why the regional population structure of V. ciliata‘is quite distinct from a metapopulation’: (i) it is difficult to define a ‘suitable’ patch; (ii) existing populations are not linked through dispersal and new populations arise through rare migration events; (iii) the persistence and spatial extent of the populations at the regional scales are very well predicted by local scale processes; and (iv) large-scale migration is probably extremely rare and population extinction rates are low. In our opinion none of these reasons is in contradiction with the system being a metapopulation. The first reason may be regarded as a methodological problem and the latter three are in fact consistent with the classical metapopulation, i.e. one that persists as a result of a stochastic balance between local extinctions and recolonizations of empty habitat patches (Levins 1969; Hanski 1999). The only thing suggested by the information provided for V. ciliata is that the colonization-extinction dynamics of the system are slow relative to the study period.

The importance of regional processes

  1. Top of page
  2. Introduction
  3. The Freckleton & Watkinson typology
  4. The importance of regional processes
  5. Is the metapopulation concept still useful for plants?
  6. Acknowledgements
  7. References

According to Freckleton & Watkinson (2002), local processes dominate the factors determining the features of plant distributions and abundance for both ‘regional ensembles’ (REs) and ‘spatially extended populations’ (SEPs). Three forms of RE are identified: ‘remnant populations’, ‘shifting clouds’ and ‘island populations’. For the first two forms it is stated that ‘the size and persistence of such populations are entirely a function of local processes’ (Freckleton & Watkinson 2002, p. 428), and for the latter form ‘emigration and recolonization play no role in the persistence of such populations’. For SEPs, of course, ‘the metapopulation notion does not apply …’. For REs and SEPs, extinctions are rare, nil or variable, recolonizations do not occur and local processes dominate to determine the features of plant distributions and abundance (Table 2 in Freckleton & Watkinson 2002). Although no quantitative assessments were made on the relative frequency of metapopulations, SEPs and the different forms of RE among plant species, the definitions of these forms of regional dynamics suggest that most plants, according to Freckleton & Watkinson (2002), display some of the latter types of dynamics (i.e. RE and SEP). Thus, a corollary is that for many plants local processes determine regional dynamics. However, an increasing number of studies document the importance of regional processes on plant distributions, also in cases where metapopulation dynamics (in a strict sense) have not been shown. If seed limitation is common in regional plant populations, as seems to be the case (reviewed by Turnbull et al. 2000), plants are likely to have difficulties in occupying available suitable habitats. If dispersal is related to distance between patches, this translates to a dependence of occupancy on habitat configuration. Most studies examining relationships between habitat area and isolation, and occupancy or colonization, indeed document such relationships (e.g. Ouborg 1993; Quintana-Ascencio & Menges 1996; Grashof-Bokdam 1997; Grashof-Bokdam & Geertsema 1998; Bastin & Thomas 1999; Harrison et al. 2000; Butaye et al. 2001; Jacquemyn et al. 2001; Dupré & Ehrlén 2002). Given this type of evidence, we think it is reasonable to conclude that for a large number of species the regional dynamics cannot be understood without consideration of extinction-colonization processes.

Interactions with pollinators and seed predators (e.g. Steffan-Dewenter et al. 2001), seed dispersers (e.g. Restrepo et al. 1999) or herbivores may be affected by habitat configuration even though the systems have no typical metapopulation dynamics. These interactions influence processes such as reproduction (e.g. Jennersten 1988; Morgan 1999; Cunningham 2000) and recruitment (e.g. Jules 1998). Inasmuch as the interactions influence plant populations, knowledge of habitat configuration and regional processes is needed to understand the dynamics of the system fully. Moreover, in remnant population systems, the actual pattern of patch occupancy may reflect previous habitat configuration. This means that the regional population cannot be modelled as a metapopulation in equilibrium with the present-day habitat configuration, but it still cannot be understood by referring to local processes alone. Knowledge of previous conditions is needed (i.e. the system has a history that needs to be considered). Lastly, in vegetation that is normally influenced by large-scale disturbances, such as wildfires (e.g. boreal forest or prairie), the effect of the disturbances may interact with the habitat configuration; for example, if patches are small they are encapsulated by the extent of the disturbances, and therefore less likely to develop a mosaic of developmental stages following disturbance. Such systems may collapse as a result of the same kind of disturbance that, under ‘unfragmented’ conditions, is necessary to maintain the system. Habitat configuration must thus be accounted for in order to understand the local response of the disturbance regime. These examples demonstrate that there are several ways in which habitat configuration may affect local populations and in which regional dynamics are not explicable from knowledge of local processes alone, even if the population system, per se, is no metapopulation.

Is the metapopulation concept still useful for plants?

  1. Top of page
  2. Introduction
  3. The Freckleton & Watkinson typology
  4. The importance of regional processes
  5. Is the metapopulation concept still useful for plants?
  6. Acknowledgements
  7. References

Freckleton & Watkinson (2002) base much of their critique of the metapopulation concept for plants on methodological problems: it is difficult to identify suitable patches, to estimate dispersal and to assess colonization and extinction. We agree that all these drawbacks to studies of regional dynamics pose severe problems. However, given that our interest is in assessing the relative importance of processes acting at different spatial and temporal scales, rather than categorizing populations, we think that a new typology is of little help. For example, statements such as ‘suitable patches may be hard to define’ (Population Type 2 ‘Regional ensembles’, Table 2 in Freckleton & Watkinson 2002) do not tell us anything about the regional dynamics of this population type. We believe that a more productive approach is to try to tackle the problems. Research on plant regional dynamics is still in its infancy, but several ways to quantify variation in suitability between patches have been suggested. Ehrlén & Eriksson (2000) used an experimental approach to assess habitat quality and occupancy patterns. Measures of environmental factors likely to be relevant for the target species, in combination with experimental sowing and transplantation, may overcome the difficulties in assessing patch suitability (thus removing one criterion for ‘regional ensembles’).

Reading the typology suggested in Table 2a of Freckleton & Watkinson (2002), and noting that for all types except ‘metapopulations’, recolonization is ‘nil’ implies that regional dynamics, in terms of extinctions and recolonizations are not at all important. We believe that the problems of estimating dispersal distances and in directly assessing colonization and extinction rates, and their relationship to landscape habitat configuration, must not deter us from trying to assess the importance of these processes in different, more indirect, ways. Improved theoretical insight into dispersal processes (e.g. Cain et al. 1998; Clark et al. 1998) will provide a breakthrough also for empirical estimates of dispersal in the field. The use of molecular markers (e.g. Ouborg et al. 1999) provides new methods for assessing seed dispersal between local populations. Although we have no solution to the problem of the short life span of humans in relation to many plants, we should acknowledge that historical data could be used to infer colonization and extinction dynamics over time periods exceeding normal research projects (e.g. Lienert et al. 2002).

In conclusion, we argue: (i) that Freckleton & Watkinson (2002) partly base their critique of the metapopulation concept for plants on too restricted an interpretation of metapopulation theory; (ii) that they make an unwarranted translation of methodological difficulties in studies of plant regional dynamics, to conceptual problems; (iii) that their suggested typology may be interpreted as if local processes are sufficient to understand regional dynamics; (iv) that available evidence in contrast suggests that local processes are insufficient for understanding regional dynamics in most plant species; (v) that the choice of temporal and spatial scale in studies may determine which ‘type’ of regional dynamics a species possesses; and (vi) that the most productive approach to studies of large-scale regional dynamics in plants is to develop the concepts of metapopulation theory, and strive towards solving problems with identification of suitable habitat, dispersal and colonization, rather than ‘defining away’ the problems by using a new typology of regional dynamics.

References

  1. Top of page
  2. Introduction
  3. The Freckleton & Watkinson typology
  4. The importance of regional processes
  5. Is the metapopulation concept still useful for plants?
  6. Acknowledgements
  7. References
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