Colonization-extinction Dynamics Research Articles

Metapopulation-level adaptation of insect host plant preference and extinction–colonization dynamics in heterogeneous landscapes

Species living in highly fragmented landscapes typically occur as metapopulations with frequent turnover of local populations. The turnover rate depends on population sizes and connectivities, but it may also depend on the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly ( Melitaea cinxia) in Finland uses two host plant species, which show variation in their relative abundances at two spatial scales: locally among individual habitat patches and regionally among networks of patches. Female butterflies in turn exhibit spatial variation in genetically determined host plant preference within and among patch networks. Emigration, immigration and establishment of new populations have all been shown to be strongly influenced by the match between the host plant composition of otherwise suitable habitat patches and the host plant preference of migrating butterflies. The evolutionary consequences of such biased migration and colonization with respect to butterfly phenotypes might differ depending on spatial configuration and plant species composition of the patches in heterogeneous patch networks. Using a spatially realistic individual-based model we show that the model-predicted evolution of host plant preference due to biased migration explains a significant amount of the observed variation in host plant use among metapopulations living in dissimilar networks. This example illustrates how the ecological extinction–colonization dynamics may be linked with the evolutionary dynamics of life history traits in metapopulations.

Probing the primacy of the patch: what makes a metapopulation?

The use of the term ‘metapopulation’ has broadened substantially since its inception to include, for example, subdivided populations that are not necessarily prone to local extinction, and populations with a locally patchy distribution that are not clearly subdivided into discrete demes. This broadened scope has coincided with an exponential increase in the number of articles applying the term (Hanski & Simberloff 1997; Pannell & Charlesworth 2000), but it has arguably come at a cost of precision. In their useful review of the literature on large-scale spatial dynamics in plants, Freckleton & Watkinson (2002) have blown the whistle on this trend. They argue that metapopulations ought only to describe an array of populations (i) that are prone to local extinction, and (ii) that also inhabit discrete and recognizable habitat patches. The first of these criteria is uncontroversial, although the rate of local population extinction that is biologically significant will depend on the nature of the questions being addressed. We believe that the second criterion, however, fails to recognize the utility of the metapopulation approach in studies that are not focused specifically on patch occupancy rates. In this sense, our view thus differs from that of Freckleton & Watkinson (2002), as well as from views expressed recently by Bullock et al . (2002), who also emphasize the importance of fixed habitat patches in defining a metapopulation. It is of course true that many applications of the metapopulation concept in ecology and conservation need to address patch occupancy rates explicitly, and thus require the a priori identification of habitat patches. In a reply to Ehrlen & Eriksson’s (2003) critique of their review, Freckleton & Watkinson (2003) emphasize this point. If we are interested in ensuring the regional conservation of a metapopulation, then efforts must be directed towards the conservation of habitat, whether currently occupied or not. But the dynamics of population turnover in a metapopulation affect not only the regional persistence or survival of a species, but also its population genetics (reviewed in Pannell & Charlesworth 2000) and evolution (reviewed in Ronce & Olivieri 2003) – whether or not we can identify its habitat. Bullock et al . (2002) state that ‘a basic premise of metapopulation theory and models [is] that extinctions make habitat patches available for colonization’ (p. 291). We agree with the implication that an empirical definition of a metapopulation ought to be consistent with its use in the theoretical literature. However, not all theoretical metapopulation models assume the existence of fixed habitat patches. It seems that our differing views stem, at least in part, from a failure to integrate genetic or evolutionary aspects of metapopulation biology with ecological or demographic ones. For example, Freckleton & Watkinson (2002) adopted an entirely demographic perspective in their review and did not consider population genetic structure, because ‘metapopulation theory is not concerned with the movement of genes per se ’ (p. 421). However, the metapopulation perspective has been used fruitfully in both ecology and population genetics, and indeed the concept was first considered by Wright (1940) in the context of population genetics long before Levins (1969, 1970) explicitly introduced the term. Ives & Whitlock (2002) have recently noted that ‘population genetic metapopulations’ may not necessarily equate with ‘ecological metapopulations’, because extinction–colonization dynamics need not affect both the demography and the genetic structure of a species to the same extent. However, because the same underlying processes make the metapopulation concept valuable in population genetics and ecology, consistency in applying the term is desirable.

Occupancy frequency distributions: patterns, artefacts and mechanisms.

Numerous hypotheses have been proposed to explain the shape of occupancy frequency distributions (distributions of the numbers of species occupying different numbers of areas). Artefactual effects include sampling characteristics, whereas biological mechanisms include organismal, niche-based and meta-population models. To date, there has been little testing of these models. In addition, although empirically derived occupancy distributions encompass an array of taxa and spatial scales, comparisons between them are often not possible because of differences in sampling protocol and method of construction. In this paper, the effects of sampling protocol (grain, sample number, extent, sampling coverage and intensity) on the shape of occupancy distributions are examined, and approaches for minimising artefactual effects recommended. Evidence for proposed biological determinants of the shape of occupancy distributions is then examined. Good support exists for some mechanisms (habitat and environmental heterogeneity), little for others (dispersal ability), while some hypotheses remain untested (landscape productivity, position in geographic range, range size frequency distributions), or are unlikely to be useful explanations for the shape of occupancy distributions 'species specificity and adaptation to habitat, extinction-colonization dynamics). The presence of a core (class containing species with the highest occupancy) mode in occupancy distributions is most likely to be associated with larger sample units, and small homogenous sampling areas positioned well within and towards the range centers of a sufficient proportion of the species in the assemblage. Satellite (class with species with the lowest occupancy) modes are associated with sampling large, heterogeneous areas that incorporate a large proportion of the assemblage range. However, satellite modes commonly also occur in the presence of a core mode, and rare species effects are likely to contribute to the presence of a satellite mode at most sampling scales. In most proposed hypotheses, spatial scale is an important determinant of the shape of the observed occupancy distribution. Because the attributes of the mechanisms associated with these hypotheses change with spatial scale, their predictions for the shape of occupancy distributions also change. To understand occupancy distributions and the mechanisms underlying them, a synthesis of pattern documentation and model testing across scales is thus needed. The development of null models, comparisons of occupancy distributions across spatial scales and taxa, documentation of the movement of individual species between occupancy classes with changes in spatial scale, as well as further testing of biological mechanisms are all necessary for an improved understanding of the distribution of species and assemblages within their geographic ranges.

Food webs in space: On the interplay of dynamic instability and spatial processes

Ecologists increasingly recognize that a consideration of spatial dynamics is essential for resolving many classical problems in community ecology. In the present paper, I argue that understanding how trophic interactions influence population stability can have important implications for the expression of spatial processes. I use two examples to illustrate this point. The first example has to do with spatial determinants of food chain length. Prior theoretical and empirical work has suggested that colonization–extinction dynamics can influence food chain length, at least for specialist consumers. I briefly review evidence and prior theory that food chain length is sensitive to area. A metacommunity scenario, in which each of various patches can have a food chain varying in length (but in which a consumer is not present on a patch unless its required resource is also present), shows that alternative landscape states are possible. This possibility arises if top predators moderate unstable interactions between intermediate predators and basal resources. The second example has to do with the impact of recurrent immigration on the stability of persistent populations. Immigration can either stabilize or destabilize local population dynamics. Moreover, an increase in immigration can decrease average population size for unstable populations with direct density‐dependence, or in predator–prey systems with saturating functional responses. These theoretical models suggest that the interplay of temporal variation and spatial fluxes can lead to novel qualitative phenomena.

Spatial Heterogeneity, Source‐Sink Dynamics, and the Local Coexistence of Competing Species

Patch occupancy theory predicts that a trade-off between competition and dispersal should lead to regional coexistence of competing species. Empirical investigations, however, find local coexistence of superior and inferior competitors, an outcome that cannot be explained within the patch occupancy framework because of the decoupling of local and spatial dynamics. We develop two-patch metapopulation models that explicitly consider the interaction between competition and dispersal. We show that a dispersal-competition trade-off can lead to local coexistence provided the inferior competitor is superior at colonizing empty patches as well as immigrating among occupied patches. Immigration from patches that the superior competitor cannot colonize rescues the inferior competitor from extinction in patches that both species colonize. Too much immigration, however, can be detrimental to coexistence. When competitive asymmetry between species is high, local coexistence is possible only if the dispersal rate of the inferior competitor occurs below a critical threshold. If competing species have comparable colonization abilities and the environment is otherwise spatially homogeneous, a superior ability to immigrate among occupied patches cannot prevent exclusion of the inferior competitor. If, however, biotic or abiotic factors create spatial heterogeneity in competitive rankings across the landscape, local coexistence can occur even in the absence of a dispersal-competition trade-off. In fact, coexistence requires that the dispersal rate of the overall inferior competitor not exceed a critical threshold. Explicit consideration of how dispersal modifies local competitive interactions shifts the focus from the patch occupancy approach with its emphasis on extinction-colonization dynamics to the realm of source-sink dynamics. The key to coexistence in this framework is spatial variance in fitness. Unlike in the patch occupancy framework, high rates of dispersal can undermine coexistence, and hence diversity, by reducing spatial variance in fitness.

Patch Dynamics and Metapopulation Theory: the Case of Successional Species

We present a mathematical framework that combines extinction–colonization dynamics with the dynamics of patch succession. We draw an analogy between the epidemiological categorization of individuals (infected, susceptible, latent and resistant) and the patch structure of a spatially heterogeneous landscape (occupied–suitable, empty–suitable, occupied–unsuitable and empty–unsuitable). This approach allows one to consider life-history attributes that influence persistence in patchy environments (e.g., longevity, colonization ability) in concert with extrinsic processes (e.g., disturbances, succession) that lead to spatial heterogeneity in patch suitability. It also allows the incorporation of seed banks and other dormant life forms, thus broadening patch occupancy dynamics to include sink habitats. We use the model to investigate how equilibrium patch occupancy is influenced by four critical parameters: colonization rate, extinction rate, disturbance frequency and the rate of habitat succession. This analysis leads to general predictions about how the temporal scaling of patch succession and extinction–colonization dynamics influences long-term persistence. We apply the model to herbaceous, early-successional species that inhabit open patches created by periodic disturbances. We predict the minimum disturbance frequency required for viable management of such species in the Florida scrub ecosystem.

Colonization-extinction dynamics of opossums on small islands in Panama

We studied the distributions and colonization-extinction dynamics of five species of opossums (Didelphis marsupialis, Marmosa robinsoni, Philander opossum, Caluromys derbianus, and Metachirus nudicaudatus) on 12 small islands in Gatun Lake in central Panama. Opossums were censused by monthly livetrapping from 1991 (eight islands) or 1993 (four islands) through 1995. We recorded 75 colonizations over the course of the study. Didelphis marsupialis was the most frequent colonizer and accounted for 56% of all colonizations recorded. However, only four D. marsupialis populations that reproduced successfully resulted from these colonizations, and most populations went extinct. Marmosa robinsoni and P. opossum also frequently colonized these islands but rarely established successful populations. Multiple linear regression was used to relate the mean numbers of colonizations and population establishments per year and mean and standardized persistence times of all five species of opossums to island size and isolation. These four dependent variables were not related to island area or isolation distance. This system, characterized by frequent colonizations and extinctions, fit the mainland-island metapopulation model, and nearby mainland areas that maintained persistent populations of all five species provided colonists to the small islands.

The importance of the relationship between population density and habitat area

The relationship between population density and habitat size, the density-area relationship, has received considerable, but often sporadic and unfocused attention (Root 1973, Risch 1981, Kareiva 1983, Bach 1988, Matter 1997). Recent reviews of the topic have revealed that there is a great deal of variability in the relationship with species showing patterns of increasing, decreasing, and constant density with habitat size (Bowers and Matter 1997, Bender et al. 1998, Connor et al. 2000). Despite this considerable variability, the overall trend across species appears to be increasing density with habitat size, especially for insects and birds (Bender et al. 1998, Connor et al. 2000; but see Gaston et al. 1999). Mammals show fairly constant densities with habitat area with about as many positive as negative density-area relationships (Bowers and Matter 1997, Connor et al. 2000). A variety of different mechanisms have been offered to account for density-area relationships. Root (1973) explained the positive density-area relationship seen for herbivorous insects in the 'resource concentration hypothesis'. He proposed that density would increase with area via dispersal if emigration rates were greater for smaller, and immigration rates were greater for larger patches (Root 1973). Subsequently, predatory rates (Risch 1981), habitat quality (Hanski 1994, Matter 1997), and social interactions (Bowers and Matter 1997, Bowers and Dooley 1999) that vary with patch size have been proposed to account for both positive and negative density-area relationships. Bowers and Matter (1997) proposed that habitat selection at small spatial scales may produce negative density-area relationships while positive relationships may arise at larger scales through colonization-extinction dynamics. Density-area relationships may also arise from methodological problems such as the mis-estimation of patch size for edge and interior species (Bender et al. 1998) or increasing amounts of non-habitat with census area (Smallwood and Schonewald 1996, Gaston et al. 1999). Gaston et al. (1999) detail many of the problems that can occur when estimating density-area relationships; however, many of the statistical problems discussed can be avoided through the use of alternative methods. Gaston et al. (1999) point out that for log density-log area plots the minimum allowable value is 1/area, which may produce a non-zero expected slope as well as heteroscedasticity. These statistical difficulties can be overcome by using an area-sensitive Poisson model (Feller 1968, Connor et al. 1997, Matter 1997). Here the expected abundance of organisms at a site is simply the mean density across all sites multiplied by site area raised to a power. This model can be fit with and without the exponent using generalized linear models to determine if density varies with area. The model has the advantage of having the appropriate variance structure and allows for the inclusion of inhabitable sites with zero density (Matter 1997). Despite research describing patterns of density with habitat area and attempting to attribute mechanisms responsible for it, researchers have yet to appreciate the importance of density-area relationships in a wider context. Similar to patterns of aggregation, density-area patterns influence a variety of ecological processes. Here, I illustrate how the density-area relationship of individual species is of fundamental importance for spatial population and community ecology and is pertinent to conservation issues.

Colonization-extinction dynamics of opossums on small islands in Panama

Colonization-extinction dynamics of opossums on small islands in Panama

Distributions and impacts of microparasites on Daphnia in a rockpool metapopulation.

We examined the spatial distributions of the microparasites on two species of Daphnia in rockpools in four areas along the coast of the Gulf of Bothnia, central Sweden. We found five taxa of parasites, of which the microsporidian Larssonia sp. occurred in all the four subareas studied, and in 44% of the pools. Other parasites, such as a microsporidian intestinal parasite of the Glugoides type and the nematode Echinura uncinata, were much less common. Larssonia had a large impact on reproduction in both Daphnia species, although D.␣longispina seemed to be somewhat less affected than D.␣pulex. We used a spatial autocorrelation method (correlogram using Moran's coefficient) to analyse the spatial distribution of the two Daphnia species and the most abundant parasite species Larssonia sp. All three species showed positive spatial autocorrelations over small distances, indicating an aggregated distribution. This suggests that colonization-extinction dynamics may be important in both host species as well as in the parasite. Larssonia showed no relation to environmental factors, while the distributions of the two Daphnia species were significantly related to the water volume of the pools. D. pulex was more often found in small pools, while D. longispina more often inhabited larger pools. Our study suggests that microparasites in rockpools have substantial effects on Daphnia demography and through this they may influence population dynamics and local extinctions.