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.     

Metapopulation dynamics of a beetle species confined to burned forest sites in a managed forest region

Despite increasing awareness of the theoretical importance of habitat dynamics on metapopulations, only a few empirical studies have been conducted. We aimed to increase our understanding of how patch size, dynamics and connectivity affect colonization–extinction dynamics and the occurrence patterns of a beetle (Stephanopachys linearis), which breeds only in burned trees, existing as dynamic habitat patches that have become rare in managed forest landscapes. We assessed species’ presence/absence twice in all known habitat patches (i.e. > 1 ha sites where forest fires had occurred during the previous 2–15 yr) in a 200 × 150 km region of central Sweden, dominated by managed boreal forest. Evaluated over six years, the colonization rate was 47% and the local extinction risk was 65%. Probability of colonization increased with patch size (number of suitable trees in a site) and connectivity to occupied patches within 30 km, and decreased with increasing time since fire. Local extinction risk decreased with habitat patch size but increased, unexpectedly, with connectivity. Occurrence increased with patch size and decreased with increasing time since fire. At a regional scale, S. linearis tracks the fire dynamics by colonising sites with burned trees and by becoming extinct at rates which make the species rare at sites where burnt trees are more than eight years old. In managed boreal forest landscapes, a large proportion of sites may be created by prescribed burning (in our study area: 82%), and consequently human decisions strongly affect the future amount of habitat for fire‐dependent species and its spatial distribution. Stephanopachys linearis uses burned sites more often if more trees are retained and, to some extent, if sites are concentrated in those parts of a region that already support high population densities of the species.     

Colonization and extinction dynamics of an annual plant metapopulation in an urban environment

The metapopulation framework considers that the spatiotemporal distribution of organisms results from a balance between the colonization and extinction of populations in a suitable and discrete habitat network. Recent spatially realistic metapopulation models have allowed patch dynamics to be investigated in natural populations but such models have rarely been applied to plants. Using a simple urban fragmented population system in which favourable habitat can be easily mapped, we studied patch dynamics in the annual plant Crepis sancta (Asteraceae). Using stochastic patch occupancy models (SPOMs) and multi‐year occupancy data we dissected extinction and colonization patterns in our system. Overall, our data were consistent with two distinct metapopulation scenarios. A metapopulation (sensu stricto) dynamic in which colonization occurs over a short distance and extinction is lowered by nearby occupied patches (rescue effect) was found in a set of patches close to the city centre, while a propagule rain model in which colonization occurs from a large external population was most consistent with data from other networks. Overall, the study highlights the importance of external seed sources in urban patch dynamics. Our analysis emphasizes the fact that plant distributions are governed not only by habitat properties but also by the intrinsic properties of colonization and dispersal of species. The metapopulation approach provides a valuable tool for understanding how colonization and extinction shape occupancy patterns in highly fragmented plant populations. Finally, this study points to the potential utility of more complex plant metapopulation models than traditionally used for analysing ecological and evolutionary processes in natural metapopulations.     

Extinction-colonization dynamics and host-plant choice in butterfly metapopulations

Species living in highly fragmented landscapes often occur as metapopulations with frequent population turnover. Turnover rate is known to depend on ecological factors, such as population size and connectivity, but it may also be influenced by the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly (Melitaea cinxia) in Finland uses two host-plant species that vary in their relative abundances among distinct habitat patches (dry meadows) in a large network of approximately 1,700 patches. We found no effect of host species use on local extinction. In contrast, population establishment was strongly influenced by the match between the host species composition of an empty habitat patch and the relative host use by larvae in previous years in the habitat patches that were well connected to the target patch. This "colonization effect" could be due to spatially variable plant acceptability or resistance or to spatially variable insect oviposition preference or larval performance. We show that spatial variation in adult oviposition preference occurs at the relevant spatial scale and that the other possible causes of the colonization effect can be discounted. We conclude that the colonization effect is generated by host preference influencing the movement patterns of ovipositing females. Migrant females with dissimilar host preferences have different perceptions of relative patch quality, which influences their likelihood of colonizing patches with particular host composition.     

Temporal genetic analysis of the endangered tidewater goby: extinction–colonization dynamics or drift in isolation?

Extinction and colonization dynamics are critical to understanding the evolution and conservation of metapopulations. However, traditional field studies of extinction–colonization are potentially fraught with detection bias and have rarely been validated. Here, we provide a comparison of molecular and field‐based approaches for assessment of the extinction–colonization dynamics of tidewater goby (Eucyclogobius newberryi) in northern California. Our analysis of temporal genetic variation across 14 northern California tidewater goby populations failed to recover genetic change expected with extinction–colonization cycles. Similarly, analysis of site occupancy data from field studies (94 sites) indicated that extinction and colonization are very infrequent for our study populations. Comparison of the approaches indicated field data were subject to imperfect detection, and falsely implied extinction–colonization cycles in several instances. For northern California populations of tidewater goby, we interpret the strong genetic differentiation between populations and high degree of within‐site temporal stability as consistent with a model of drift in the absence of migration, at least over the past 20–30 years. Our findings show that tidewater goby exhibit different population structures across their geographic range (extinction–colonization dynamics in the south vs. drift in isolation in the north). For northern populations, natural dispersal is too infrequent to be considered a viable approach for recolonizing extirpated populations, suggesting that species recovery will likely depend on artificial translocation in this region. More broadly, this work illustrates that temporal genetic analysis can be used in combination with field data to strengthen inference of extinction–colonization dynamics or as a stand‐alone tool when field data are lacking.     

How patch configuration affects the impact of disturbances on metapopulation persistence

Disturbances affect metapopulations directly through reductions in population size and indirectly through habitat modification. We consider how metapopulation persistence is affected by different disturbance regimes and the way in which disturbances spread, when metapopulations are compact or elongated, using a stochastic spatially explicit model which includes metapopulation and habitat dynamics. We discover that the risk of population extinction is larger for spatially aggregated disturbances than for spatially random disturbances. By changing the spatial configuration of the patches in the system--leading to different proportions of edge and interior patches--we demonstrate that the probability of metapopulation extinction is smaller when the metapopulation is more compact. Both of these results become more pronounced when colonization connectivity decreases. Our results have important management implication as edge patches, which are invariably considered to be less important, may play an important role as disturbance refugia.     

Metapopulation extinction thresholds in rain forest remnants

Although habitat fragmentation is a major threat to global biodiversity, the demographic mechanisms underlying species loss from tropical forest remnants remain largely unexplored. In particular, no studies at the landscape scale have quantified fragmentation's impacts on colonization, extinction, and local population growth simultaneously. In central Amazonia, we conducted a multiyear demographic census of 292 populations of two leaf-inhabiting (i.e., epiphyllous) bryophyte species transplanted from continuous forest into a network of 10 study sites ranging from 1, 10, and 100 to > 10,000 ha in size. All populations experienced significantly positive local growth (lambda > 1) and a nearly constant per-generational extinction probability (15%). However, experimental leaf patches in reserves of > or = 100 ha experienced nearly double (48%) the colonization probability observed in small reserves (27%), suggesting that the proximate cause of epiphyll species loss in small fragments (< or = 10 ha) is reduced colonization. Nonetheless, populations of small fragments exhibit rates of colonization above patch extinction, positive local growth, and low temporal variation, which are features that should theoretically reduce the probability of extinction. This result suggests that for habitat-tracking metapopulations subject to frequent and stochastic turnover events, including epiphylls, colonization/extinction ratios must be maintained well above unity to ensure metapopulation persistence.     

On the neutrality of molecular genetic markers: pedigree analysis of genetic variation in fragmented populations

Many studies employ molecular markers to infer ecological and evolutionary processes, assuming that variation found at genetic loci offers a reliable representation of stochastic events in natural populations. Increasingly, evidence emerges that molecular markers might not always be selectively neutral. However, only a few studies have analysed how deviations from neutrality could affect estimates of genetic variation, using populations with known genealogy. We monitored changes in allozyme variation over eight generations in captive metapopulations of the butterfly Bicyclus anynana. Population demography was recorded by individually marking 35 000 butterflies and constructing pedigrees. We designed a computer program that simulated the inheritance of founder allozyme alleles in butterfly pedigrees. We thus tested whether the observed transmission of allozyme alleles could be explained by random genetic drift alone, or whether there was evidence for positive or negative selection. This analysis showed that in the smallest metapopulations the loss of allozyme variation exceeded the neutral rate. Possibly, linkage disequilibria between deleterious mutations and marker alleles resulted in background selection and a faster erosion of allozyme variation. In larger metapopulations, one locus (MDH) showed a significant heterozygote excess and smaller than expected loss in heterozygosity, observations consistent with (associative) overdominance. This study demonstrates that the neutrality of molecular markers cannot always be assumed, particularly in small populations with a high mutation load.     

Testing metapopulation concepts: effects of patch characteristics and neighborhood occupancy on the dynamics of an endangered lagomorph

Metapopulation ecology is a field that is richer in theory than in empirical results. Many existing empirical studies use an incidence function approach based on spatial patterns and key assumptions about extinction and colonization rates. Here we recast these assumptions as hypotheses to be tested using 18 years of historic detection survey data combined with four years of data from a new monitoring program for the Lower Keys marsh rabbit. We developed a new model to estimate probabilities of local extinction and colonization in the presence of nondetection, while accounting for estimated occupancy levels of neighboring patches. We used model selection to identify important drivers of population turnover and estimate the effective neighborhood size for this system. Several key relationships related to patch size and isolation that are often assumed in metapopulation models were supported: patch size was negatively related to the probability of extinction and positively related to colonization, and estimated occupancy of neighboring patches was positively related to colonization and negatively related to extinction probabilities. This latter relationship suggested the existence of rescue effects. In our study system, we inferred that coastal patches experienced higher probabilities of extinction and colonization than interior patches. Interior patches exhibited higher occupancy probabilities and may serve as refugia, permitting colonization of coastal patches following disturbances such as hurricanes and storm surges. Our modeling approach should be useful for incorporating neighbor occupancy into future metapopulation analyses and in dealing with other historic occupancy surveys that may not include the recommended levels of sampling replication.     

Generalizing Levins metapopulation model in explicit space: models of intermediate complexity

A recent study [Harding and McNamara, 2002. A unifying framework for metapopulation dynamics. Am. Nat. 160, 173-185] presented a unifying framework for the classic Levins metapopulation model by incorporating several realistic biological processes, such as the Allee effect, the Rescue effect and the Anti-rescue effect, via appropriate modifications of the two basic functions of colonization and extinction rates. Here we embed these model extensions on a spatially explicit framework. We consider population dynamics on a regular grid, each site of which represents a patch that is either occupied or empty, and with spatial coupling by neighborhood dispersal. While broad qualitative similarities exist between the spatially explicit models and their spatially implicit (mean-field) counterparts, there are also important differences that result from the details of local processes. Because of localized dispersal, spatial correlation develops among the dynamics of neighboring populations that decays with distance between patches. The extent of this correlation at equilibrium differs among the metapopulation types, depending on which processes prevail in the colonization and extinction dynamics. These differences among dynamical processes become manifest in the spatial pattern and distribution of “clusters” of occupied patches. Moreover, metapopulation dynamics along a smooth gradient of habitat availability show significant differences in the spatial pattern at the range limit. The relevance of these results to the dynamics of disease spread in metapopulations is discussed.     

Dances with fire: Tracking metapopulation dynamics of<Emphasis Type="Italic">polygonella basiramia</Emphasis> in Florida scrub (USA)

The regional persistence of species subject to local population colonization and extinction necessarily depends on how landscape features and disturbance affect metapopulation dynamics. Here, we characterize the metapopulation structure and short-term dynamics ofPolygonella basiramia. This rare, short-lived perennial herb is endemic to Florida scrublands and lacks a seed bank. Fires create the open sand gaps within a shrub matrix that support this species but also kill established plants. Thus, persistence depends on frequent colonization of unoccupied gaps. We are monitoring population dynamics within and among 1204 gaps distributed among 19 shrub patches. Considerable subpopulation turnover is evident at the gap level with rates of gap extinction exceeding rates of colonization in the first year. Whether declines in overall abundance continue is likely to depend on patterns of disturbance and regional stochasticity in this dynamic landscape.Polygonella is more likely to occupy larger and less isolated gaps, demonstrating that landscape features and disturbance strongly affect metapopulation dynamics. BecausePolygonella basiramia displays characteristics, occupancy patterns, and turnover dynamics consistent with metapopulation theory, it represents a model system for studying plant metapopulations.     

Structured models of metapopulation dynamics

I develop models of metapopulation dynamics that describe changes in the numbers of individuals within patches. These models are analogous to structured population models, with patches playing the role of individuals. Single species models which do not include the effect of immigration on local population dynamics of occupied patches typically lead to a unique equilibrium. The models can be used to study the distributions of numbers of individuals among patches, showing that both metapopulations with local outbreaks and metapopulations without outbreaks can occur in systems with no underlying environmental variability. Distributions of local population sizes (in occupied patches) can vary independently of the total population size, so both patterns of distributions of local population sizes are compatible with either rare or common species. Models which include the effect of immigration on local population dynamics can lead to two positive equilibria, one stable and one unstable, the latter representing a threshold between regional extinction and persistence.     

Effects of experimental population extinction for the spatial population dynamics of the butterfly Parnassius smintheus

While many studies have examined factors potentially impacting the rate of local population extinction, few experimental studies have examined the consequences of extinction for spatial population dynamics. Here we report results from a large‐scale, long‐term experiment examining the effects of local population extinction for the dynamics of surrounding populations. From 2001–2008 we removed all adult butterflies from two large, neighboring populations within a system of 17 subpopulations of the Rocky Mountain Apollo butterfly, Parnassius smintheus. Surrounding populations were monitored using individual, mark–recapture methods. We found that population removal decreased immigration to surrounding populations in proportion to their connectivity to the removed populations. Correspondingly, within‐generation population abundance declined. Despite these effects, we saw little consistent impact between generations. The extinction rates of surrounding populations were unaffected and local population growth was not consistently reduced by the lack of immigration. The broader results show that immigration affects local abundance within generations, but dynamics are mediated by density‐dependence within populations and by broader density‐independent factors acting between generations. The loss of immigrants resulting from extinction has little impact on the persistence of local populations in this system.     

Incidence and population dynamics of the leaf beetle Gonioctena olivacea in dynamic habitats

In natural as well as in cultural landscapes, disturbance and succession are responsible for the emergence and subsequent disappearance of suitable habitat patches. The dynamics of habitat patches has important consequences for the spatial structure and dynamics of regional populations. However, there are only few studies quantifying both patch dynamics and incidence of insect species in a dynamic landscape over several years. I studied the incidence and population dynamics of the leaf beetle Gonioctena olivacea in a system of dynamic patches of the host plant Scotch broom Cytisus scoparius . The incidence of the beetle was most strongly affected by patch area, whereas connectivity, patch quality, patch age, and landscape context had no or only a minor effect when analysed with logistic regression. The size of local beetle populations was highly fluctuating between the years; however, the population dynamics of the local populations was not synchronous. Adjacent patches did not show higher degrees of synchrony than patches separated by large distances. In the three years of study, local populations became extinct through demographic or environmental stochasticity and patch destruction. Each year >10% of the patches disappeared. The extinction rate of beetles in persistent patches was decreasing with increasing patch area. On the other hand, patches newly emerged and were rapidly colonized by the beetle. The colonization rate depended on patch connectivity. Obviously, Gonioctena olivacea was capable of persisting in this system with high turnover of patches owing to its high dispersal power.     

Colonization–extinction dynamics of epixylic lichens along a decay gradient in a dynamic landscape

Metapopulation models are often used for understanding and predicting species dynamics in fragmented landscapes. Several models have been proposed depending on e.g. the relative importance of patch dynamics on the metapopulation dynamics. Dead wood is a dynamic substrate patch, and species that are confined to such patches have experienced a high degree of habitat loss in managed forests. Little is, however, known about how the population dynamics of epixylic species are affected by the fast dynamics of their substrate patches. We quantified the effect of local patch conditions and metapopulation processes on colonizations and extinctions of epixylic lichen species in a managed boreal forest landscape. This was done by twice surveying seven lichen metapopulations on 293 stumps in 30 stands of ages covering the duration of the dynamic patches (stumps). We also investigated the relative importance of local stochastic extinctions from stumps that remained available, and deterministic extinctions due to stump surface disappearance. We found importance of a decay gradient, surrounding metapopulation size, and local population sizes, in driving the colonization–extinction dynamics of epixylic lichens. The species were sorted along the stump decay gradient. Increasing surrounding metapopulation size was associated with increased colonization rates, and increasing local population size decreased lichen extinction rates. Finally, both local stochastic extinctions and deterministic extinctions due to patch disappearance occur, confirming that the long‐term persistence of epixylic lichens depends on colonization rates that compensate for stochastic population extinctions as well as deterministic extinctions.     

Metapopulation models for seasonally migratory animals

Metapopulation models are widely used to study species that occupy patchily distributed habitat, but are rarely applied to migratory species, because of the difficulty of identifying demographically independent subpopulations. Here, we extend metapopulation theory to describe the directed seasonal movement of migratory populations between two sets of habitat patches, breeding and non-breeding, with potentially different colonization and extinction rates between patch types. By extending the classic metapopulation model, we show that migratory metapopulations will persist if the product of the two colonization rates exceeds the product of extinction rates. Further, we develop a spatially realistic migratory metapopulation model and derive a landscape metric-the migratory metapopulation capacity-that determines persistence. This new extension to metapopulation theory introduces an important tool for the management and conservation of migratory species and may also be applicable to model the dynamics of two host-parasite systems.     

Nestedness of butterfly assemblages in the Zhoushan Archipelago,China: area effects,life-history traits and conservation implications

The nested subset pattern (nestedness) of faunal assemblages has been a research focus in the fields of island biogeography and conservation biology in recent decades. However, relatively few studies have described nestedness in butterfly assemblages in oceanic archipelago systems. Moreover, previous studies often quantified nestedness using inappropriate nestedness metrics and random fill algorithms with high Type I errors. The aims of this study are to examine the existence of nestedness and underlying causal mechanisms of butterfly assemblages in the Zhoushan Archipelago, China. We used the line-transect method to determine butterfly occupancy and abundance on 42 study islands from July to August 2014. We obtained butterfly life-history traits (wingspan, body weight and minimum area requirement) by field work and island geographical features (area and isolation) from the literature. We used the recently developed metric WNODF to estimate nestedness. Partial Spearman rank correlation was used to evaluate the associations of nestedness and island geographical features as well as butterfly life-history traits related to species extinction risk and colonization ability. The butterfly assemblages were significantly nested. Island area and minimum area requirement of butterflies were significantly correlated with nestedness after controlling for other independent variables. In contrast, the nestedness of butterflies did not appear to result from passive sampling or selective colonization. However, multi-year studies are needed to confirm that target effects are not muddling these results. Our results indicate that selective extinction may be the main driver of nestedness of butterfly assemblages in our study system. From a conservation viewpoint, we should protect both large islands and species with large area requirement to maximize the number of species preserved.     

Correlated extinctions, colonizations and population fluctuations in a highly connected ringlet butterfly metapopulation

 The persistence of metapopulations is likely to be highly dependent on whether population dynamics are correlated among habitat patches as a result of migration between patches and spatially-correlated environmental stochasticity (weather effects). We examined whether population dynamics of the ringlet butterfly, Aphantopus hyperantus, were synchronous in an area of approximately 0.5 km², with respect to extinction, colonization and population fluctuations. Monks Wood Butterfly Monitoring Scheme transect count data from 1973 to 1995, revealed (A) a major environmental perturbation, the drought of 1976, which caused synchronized extinctions of A. hyperantus in subsequent years, (B) synchronized recolonization in years following the large number of apparent extinctions, and (C) population changes by A. hyperantus were highly correlated in many of the 14 sections of the transect, presumably reflecting similar responses to environmental stochasticity, and the exchange of individuals among sections. However, extinction and population synchrony depended on habitat type. Following the 1976 drought, A. hyperantus apparently became extinct from the most open and most shady habitats it occupied, with some persistence in habitats of intermediate shading, thus showing retraction to core populations in central parts of an environmental gradient, albeit with an average shift to relatively open habitat. Populations at extreme ends of the environmental gradient occupied by A. hyperantus fluctuated least synchronously, suggesting a potential buffering effect of habitat heterogeneity, but this was not crucial to survival after the 1976 drought. Thus, not all habitats are equally important to persistence. Correlated temporal dynamics, variation in habitat quality and the interaction between habitat quality and temporal environmental stochasticity are important determinants of metapopulation persistence and should be incorporated in metapopulation models. Received: 26 April 1996 / Accepted: 17 July 1996     

Stability aware spatial cut of metapopulations ecological networks

Ecological complex networks are common in the study of patched ecological systems where evolving populations interact within and among the patches. The loss of the dispersal connections between patches due to reasons such as erosion of migration corridors and road construction can cause an undesirable partitioning of such networks resulting in instability or negative impact on the metapopulations. A partitioning or spatial cut that is aware of the stability of the dynamics in the resulting daughter sub-networks can be an effective tool in dealing with the situation like proposing road alignment through a metapopulations network. This paper provides some mathematical conditions along with an heuristic graph partitioning algorithm that can help in finding ecologically suitable partitions of the metapopulations networks. Our study noted the crucial role of network connectivity (measured by Fiedler value) in stabilizing the metapopulations. That is, a sufficiently connected metapopulations network along with constrained internal patch dynamics has stable dynamics around its homogeneous co-existential equilibrium solution. With the considered mathematical model in this paper, network partitioning does not alter the internal patch dynamics around its homogeneous equilibrium point, but it can change the connectivity levels in the partitioned subnetworks. Thus, the proposed partitioning problem for an already stable metapopulations network is reduced to finding its subnetworks with desirable connectivity levels.