Metapopulation Persistence in Random Fragmented Landscapes

Habitat destruction and land use change are making the world in which natural populations live increasingly fragmented, often leading to local extinctions. Although local populations might undergo extinction, a metapopulation may still be viable as long as patches of suitable habitat are connected by dispersal, so that empty patches can be recolonized. Thus far, metapopulations models have either taken a mean-field approach, or have modeled empirically-based, realistic landscapes. Here we show that an intermediate level of complexity between these two extremes is to consider random landscapes, in which the patches of suitable habitat are randomly arranged in an area (or volume). Using methods borrowed from the mathematics of Random Geometric Graphs and Euclidean Random Matrices, we derive a simple, analytic criterion for the persistence of the metapopulation in random fragmented landscapes. Our results show how the density of patches, the variability in their value, the shape of the dispersal kernel, and the dimensionality of the landscape all contribute to determining the fate of the metapopulation. Using this framework, we derive sufficient conditions for the population to be spatially localized, such that spatially confined clusters of patches act as a source of dispersal for the whole landscape. Finally, we show that a regular arrangement of the patches is always detrimental for persistence, compared to the random arrangement of the patches. Given the strong parallel between metapopulation models and contact processes, our results are also applicable to models of disease spread on spatial networks.     

Habitat quality of source patches and connectivity in fragmented landscapes

Because spatial connectivity is critical to dispersal success and persistence of species in highly fragmented landscapes, the way that we envision and measure connectivity is consequential for biodiversity conservation. Connectivity metrics used for predictive modeling of spatial turnover and patch occupancy for metapopulations, such as with Incidence Function Models (IFM), incorporate distances to and sizes of possible source populations. Here, our focus is on whether habitat quality of source patches also is considered in these connectivity metrics. We propose that effective areas (weighted by habitat quality) of source patches should be better surrogates for population size and dispersal potential compared to unadjusted patch areas. Our review of a representative sample of the literature revealed that only 12.5% of studies incorporated habitat quality of source patches into IFM-type connectivity metrics. Quality of source patches generally was not taken into account in studies even if habitat quality of focal patches was included in analyses. We provide an empirical example for a metapopulation of a rare wetland species, the round-tailed muskrat (Neofiber alleni), demonstrating that a connectivity metric based on effective areas of source patches better predicts patch colonization and occupancy than a metric that used simple patch areas. The ongoing integration of landscape ecology and metapopulation dynamics could be hastened by incorporating habitat quality of source patches into spatial connectivity metrics applied to species conservation in fragmented landscapes.     

Effects of local and landscape factors on the abundance of an endangered multivoltine butterfly at riverbanks

Plebejus argyrognomon is one of the grassland‐dwelling butterflies undergoing rapid decline in recent decades. Grassland habitats for butterflies are generally threatened by fragmentation and invasive species, hence are among the most vulnerable ecosystems. We studied the seasonal abundance of P. argyrognomon at habitat patches along the banks of the Kinugawa River in eastern Japan, to identify environmental factors suitable for population persistence of this species, including habitat patch connectivity. Results showed that the patch's host plant cover had a positive effect on abundance in all three seasons, while the shading of the host plants by surrounding non‐host plants and nearby forested area showed negative effects. Additionally, habitat patch connectivity and nectar richness could be considered as positive factors in autumn and summer, respectively. Analysis of habitat connectivity also showed that the Kinugawa River did not appear to act as a dispersal barrier for P. argyrognomon. Our findings emphasize the importance of understanding environmental factors that may vary among seasons, and such understanding could contribute to habitat management of multivoltine butterflies in fragmented landscapes.     

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.     

How does temporal variation in habitat connectivity influence metapopulation dynamics?

Metapopulation persistence depends on connectivity between habitat patches. While emphasis has been placed on the spatial dynamics of connectivity, much less has been placed on its short‐term temporal dynamics. In many terrestrial and aquatic ecosystems, however, transient (short‐term) changes in connectivity occur as habitat patches are connected and disconnected due, for example, to climatic or hydrological variability. We evaluated the implications of transient connectivity using a network‐based metapopulation model and a series of scenarios representing temporal changes in connectivity. The transient loss of connectivity can influence metapopulation persistence, and more strongly autocorrelated temporal dynamics affect metapopulation persistence more severely. Given that many ecosystems experience short‐term and temporary loss of habitat connectivity, it is important that these dynamics are adequately represented in metapopulation models; failing to do so may yield overly optimistic‐estimates of metapopulation persistence in fragmented landscapes.     

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.     

Prioritization of landscape connectivity for the conservation of Peary caribou

Adequate connectivity between discontinuous habitat patches is crucial for the persistence of metapopulations across space and time. Loss of landscape connectivity is often a direct result of fragmentation caused by human activities but also can be caused indirectly through anthropogenic climate change. Peary caribou (Rangifer tarandus pearyi) are widely dispersed across the islands of the Canadian Arctic Archipelago and rely on sea ice to move seasonally between island habitats throughout their range. Seasonal connectivity provided by sea ice is necessary to maintain genetic diversity and to facilitate dispersal and recolonization of areas from which caribou have been extirpated. We used least‐cost path analysis and circuit theory to model connectivity across Peary caribou range, and future climate projections to investigate how this connectivity might be affected by a warming climate. Further, we used measures of current flow centrality to estimate the role of High Arctic islands in maintaining connectivity between Peary caribou populations and to identify and prioritize those islands and linkages most important for conservation. Our results suggest that the Bathurst Island complex plays a critical role in facilitating connectivity between Peary caribou populations. Large islands, including Banks, Victoria, and Ellesmere have limited roles in connecting Peary caribou. Without rigorous greenhouse gas emission reductions our projections indicate that by 2100 all connectivity between the more southern Peary caribou populations will be lost for important spring and early‐winter movement periods. Continued connectivity across the Canadian Arctic Archipelago, and possibly Peary caribou persistence, ultimately hinges on global commitments to limit climate change. Our research highlights priority areas where, in addition to emission reductions, conservation efforts to maintain connectivity would be most effective.     

Gene flow and functional connectivity in the natterjack toad

Functional connectivity is a key factor for the persistence of many specialist species in fragmented landscapes. However, connectivity estimates have rarely been validated by the observation of dispersal movements. In this study, we estimated functional connectivity of a real landscape by modelling dispersal for the endangered natterjack toad (Bufo calamita) using cost distance. Cost distance allows the evaluation of 'effective distances', which are distances corrected for the costs involved in moving between habitat patches in spatially explicit landscapes. We parameterized cost-distance models using the results of our previous experimental investigation of natterjack's movement behaviour. These model predictions (connectivity estimates from the GIS study) were then confronted to genetic-based dispersal rates between natterjack populations in the same landscape using Mantel tests. Dispersal rates between the populations were inferred from variation at six microsatellite loci. Based on these results, we conclude that matrix structure has a strong effect on dispersal rates. Moreover, we found that cost distances generated by habitat preferences explained dispersal rates better than did the Euclidian distances, or the connectivity estimate based on patch-specific resistances (patch viscosity). This study is a clear example of how landscape genetics can validate operational functional connectivity estimates.     

Experimental beetle metapopulations respond positively to dynamic landscapes and reduced connectivity

Interactive effects of multiple environmental factors on metapopulation dynamics have received scant attention. We designed a laboratory study to test hypotheses regarding interactive effects of factors affecting the metapopulation dynamics of red flour beetle, Tribolium castaneum. Within a four-patch landscape we modified resource level (constant and diminishing), patch connectivity (high and low) and patch configuration (static and dynamic) to conduct a 2(3) factorial experiment, consisting of 8 metapopulations, each with 3 replicates. For comparison, two control populations consisting of isolated and static subpopulations were provided with resources at constant or diminishing levels. Longitudinal data from 22 tri-weekly counts of beetle abundance were analyzed using bayesian Poisson generalized linear mixed models to estimate additive and interactive effects of factors affecting abundance. Constant resource levels, low connectivity and dynamic patches yielded greater levels of adult beetle abundance. For a given resource level, frequency of colonization exceeded extinction in landscapes with dynamic patches when connectivity was low, thereby promoting greater patch occupancy. Negative density dependence of pupae on adults occurred and was stronger in landscapes with low connectivity and constant resources; these metapopulations also demonstrated greatest stability. Metapopulations in control landscapes went extinct quickly, denoting lower persistence than comparable landscapes with low connectivity. When landscape carrying capacity was constant, habitat destruction coupled with low connectivity created asynchronous local dynamics and refugia within which cannibalism of pupae was reduced. Increasing connectivity may be counter-productive and habitat destruction/recreation may be beneficial to species in some contexts.     

Structure and fragmentation of growling grass frog metapopulations

Metapopulations occur in fragmented landscapes, and consist of demographically-independent populations connected by dispersal. Nevertheless, anthropogenic habitat fragmentation may be fatal to metapopulations, as it disrupts dispersal and gene flow, and undermines the balance between population extinction and colonization. Understanding the extent to which particular land-use practices disrupt dispersal and gene flow is therefore crucial for conserving metapopulations. We examined the structure and fragmentation of metapopulations of the endangered growling grass frog (Litoria raniformis) in an urbanizing landscape in southern Australia. Population clustering analyses revealed three distinct genetic units, corresponding to the three wetland clusters sampled. Isolation-by-distance was apparent between populations, and genetic distance was significantly correlated with the presence of urban barriers between populations. Our study provides evidence that urbanization fragments metapopulations of L. raniformis. Managers of L. raniformis in urbanizing landscapes should seek to mitigate effects of urbanization on dispersal and gene flow.     

Invasion and persistence of infectious agents in fragmented host populations

One of the important questions in understanding infectious diseases and their prevention and control is how infectious agents can invade and become endemic in a host population. A ubiquitous feature of natural populations is that they are spatially fragmented, resulting in relatively homogeneous local populations inhabiting patches connected by the migration of hosts. Such fragmented population structures are studied extensively with metapopulation models. Being able to define and calculate an indicator for the success of invasion and persistence of an infectious agent is essential for obtaining general qualitative insights into infection dynamics, for the comparison of prevention and control scenarios, and for quantitative insights into specific systems. For homogeneous populations, the basic reproduction ratio R(0) plays this role. For metapopulations, defining such an 'invasion indicator' is not straightforward. Some indicators have been defined for specific situations, e.g., the household reproduction number R*. However, these existing indicators often fail to account for host demography and especially host migration. Here we show how to calculate a more broadly applicable indicator R(m) for the invasion and persistence of infectious agents in a host metapopulation of equally connected patches, for a wide range of possible epidemiological models. A strong feature of our method is that it explicitly accounts for host demography and host migration. Using a simple compartmental system as an example, we illustrate how R(m) can be calculated and expressed in terms of the key determinants of epidemiological dynamics.     

Transcriptome Analysis Reveals Signature of Adaptation to Landscape Fragmentation

We characterize allelic and gene expression variation between populations of the Glanville fritillary butterfly (Melitaea cinxia) from two fragmented and two continuous landscapes in northern Europe. The populations exhibit significant differences in their life history traits, e.g. butterflies from fragmented landscapes have higher flight metabolic rate and dispersal rate in the field, and higher larval growth rate, than butterflies from continuous landscapes. In fragmented landscapes, local populations are small and have a high risk of local extinction, and hence the long-term persistence at the landscape level is based on frequent re-colonization of vacant habitat patches, which is predicted to select for increased dispersal rate. Using RNA-seq data and a common garden experiment, we found that a large number of genes (1,841) were differentially expressed between the landscape types. Hexamerin genes, the expression of which has previously been shown to have high heritability and which correlate strongly with larval development time in the Glanville fritillary, had higher expression in fragmented than continuous landscapes. Genes that were more highly expressed in butterflies from newly-established than old local populations within a fragmented landscape were also more highly expressed, at the landscape level, in fragmented than continuous landscapes. This result suggests that recurrent extinctions and re-colonizations in fragmented landscapes select a for specific expression profile. Genes that were significantly up-regulated following an experimental flight treatment had higher basal expression in fragmented landscapes, indicating that these butterflies are genetically primed for frequent flight. Active flight causes oxidative stress, but butterflies from fragmented landscapes were more tolerant of hypoxia. We conclude that differences in gene expression between the landscape types reflect genomic adaptations to landscape fragmentation.     

Between‐patch natal dispersal declines with increasing natal patch size and distance to other patches in the endangered Southern Dunlin Calidris alpina schinzii

Natal dispersal has profound consequences for populations through the movement of individuals and genes. Habitat fragmentation reduces structural connectivity by decreasing patch size and increasing isolation, but understanding of how this impacts dispersal and the functional connectivity of landscapes is limited because many studies are constrained by the size of the study areas or sample sizes to accurately capture natal dispersal. We quantified natal dispersal probability and natal dispersal distances in a small migratory shorebird, the Southern Dunlin Calidris alpina schinzii, with data from two extensively monitored endangered metapopulations breeding in Sweden and Finland. In both metapopulations philopatry was strong, with individuals returning to or close to their natal patches more often than expected by chance, consistent with the patchy distribution of their breeding habitat. Dispersal probabilities were lower and dispersal distances were shorter in Sweden. These results provide a plausible explanation for the observed inbreeding and population decline of the Swedish population. The differences between Sweden and Finland were explained by patch‐specific differences. Between‐patch dispersal decreased with increasing natal patch size and distance to other patches. Our results suggest that reduced connectivity reduces movements of the philopatric Dunlin, making it vulnerable to the effects of inbreeding. Increasing connectivity between patches should thus be one of the main goals when planning future management. This may be facilitated by creating a network of suitably sized patches (20–100 ha), no more than 20 km apart from each other, from existing active patches that may work as stepping stones for movement, and by increasing nest success and pre‐fledging survival in small patches.     

Long-term persistence of midsized to large-bodied mammals in Amazonian landscapes under varying contexts of forest cover

Both forest fragmentation and overhunting have profound effects on the structure of large-vertebrate assemblages in neotropical forests. However, the long-term value of habitat fragments for forest mammals remains poorly understood and few regional scale studies have replicated sampling across spatially independent landscapes. Here, we assess the species occupancy and abundance of midsized to large-bodied mammals within three neighbouring Amazonian forest landscapes varying widely in extent of forest cover. One of these consisted of forest fragments surrounded by semi-natural scrub savannahs that had been occupied by paleoindian populations for at least 7,000 years, whereas forest cover in the other two landscapes was either variegated or continuous. Data on species occurrence and abundance from diurnal and nocturnal line-transect surveys and local interviews in each landscape were used to examine the effects of forest cover and hunting pressure on mammal persistence within forest patches. The extent of forest cover was a key determinant of species persistence across the three landscapes, but populations of large-bodied species were either reduced or driven to local extinction by hunting even in the most forested and least fragmented landscape. Many game and non-game species persisted in forest isolates, even though, individually, these were likely too small to support viable populations. This study indicates that even small, long-term forest fragments may retain significant conservation value if they can be managed within the context of enhanced connectivity across wider fragmented landscapes.     

Connectivity compensates for low habitat quality and small patch size in the butterfly <Emphasis Type="Italic">Cupido minimus</Emphasis>

Habitat size, habitat isolation and habitat quality are regarded as the main determinants of butterfly occurrence in fragmented landscapes. To analyze the relationship between the occurrence of the butterfly Cupido minimus and these factors, patch occupancy of the immature stages in patches of its host plant Anthyllis vulneraria was studied in the nature reserve Hohe Wann in Bavaria (Germany). In 2001 and 2002, 82 A. vulneraria patches were surveyed for the presence of C. minimus larvae. The occurrence was largely affected by the size of the food plant patches. In a habitat model that uses multiple logistic regression, the type of management and habitat connectivity are further determinants of species distribution. Internal and temporal validation demonstrate the stability and robustness of the developed habitat models. Additionally, it was proved that the colonization rate of C. minimus was significantly influenced by the distance to the next occupied Anthyllis patch. Concerning long-term survival of (meta-) populations in fragmented landscapes, the results show that lower habitat quality may be compensated by higher connectivity between host plant patches. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effects of colonization asymmetries on metapopulation persistence

Ocean currents, prevailing winds, and the hierarchical structures of river networks are known to create asymmetries in re-colonization between habitat patches. The impacts of such asymmetries on metapopulation persistence are seldom considered, especially rarely in theoretical studies. Considering three classical models (the island, the stepping stone and the distance-dependent model), we explore how metapopulation persistence is affected by (i) asymmetry in dispersal strength, in which the colonization rate between two patches differs in direction, and (ii) asymmetry in connectivity, in which the overall colonization pattern displays asymmetry (circulating or dendritic networks). Viability can be drastically reduced when directional bias in dispersal strength is higher than 25%. Re-colonization patterns that allow for strong local connectivity provide the highest persistence compared to systems that allow circulation. Finally, asymmetry has relatively weak effects when metapopulations maintain strong general connectivity.     

Comparative Population Genetic Structure of the Endangered Southern Brown Bandicoot,Isoodon obesulus,in Fragmented Landscapes of Southern Australia

Genetic connectivity is a key factor for maintaining the persistence of populations in fragmented landscapes. In highly modified landscapes such us peri-urban areas, organisms’ dispersal among fragmented habitat patches can be reduced due to the surrounding matrix, leading to subsequent decreased gene flow and increased potential extinction risk in isolated sub-populations. However, few studies have compared within species how dispersal/gene flow varies between regions and among different forms of matrix that might be encountered. In the current study, we investigated gene flow and dispersal in an endangered marsupial, the southern brown bandicoot (Isoodon obesulus) in a heavily modified peri-urban landscape in South Australia, Australia. We used 14 microsatellite markers to genotype 254 individuals which were sampled from 15 sites. Analyses revealed significant genetic structure. Our analyses also indicated that dispersal was mostly limited to neighbouring sites. Comparisons of these results with analyses of a different population of the same species revealed that gene flow/dispersal was more limited in this peri-urban landscape than in a pine plantation landscape approximately 400 km to the south-east. These findings increase our understanding of how the nature of fragmentation can lead to profound differences in levels of genetic connectivity among populations of the same species.     

Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus

Rodent host dynamics and dispersal are thought to be critical for hantavirus epidemiology as they determine pathogen persistence and transmission within and between host populations. We used landscape genetics to investigate how the population dynamics of the bank vole Myodes glareolus, the host of Puumala hantavirus (PUUV), vary with forest fragmentation and influence PUUV epidemiology. We sampled vole populations within the Ardennes, a French PUUV endemic area. We inferred demographic features such as population size, isolation and migration with regard to landscape configuration. We next analysed the influence of M. glareolus population dynamics on PUUV spatial distribution. Our results revealed that the global metapopulation dynamics of bank voles were strongly shaped by landscape features, including suitable patch size and connectivity. Large effective size in forest might therefore contribute to the higher observed levels of PUUV prevalence. By contrast, populations from hedge networks highly suffered from genetic drift and appeared strongly isolated from all other populations. This might result in high probabilities of local extinction for both M. glareolus and PUUV. Besides, we detected signatures of asymmetric bank vole migration from forests to hedges. These movements were likely to sustain PUUV in fragmented landscapes. In conclusion, our study provided arguments in favour of source‐sink dynamics shaping PUUV persistence and spread in heterogeneous, Western European temperate landscapes. It illustrated the potential contribution of landscape genetics to the understanding of the epidemiological processes occurring at this local scale.     

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.     

Frog survival and population viability in an agricultural landscape with a drying climate

Amphibians are the most threatened class of vertebrate in the world. Although a number of causes of the amphibian decline phenomenon are emerging, there is a need for robust demographic data to be able to monitor current and future threats such as climate change. Despite this, few studies on amphibians have the life-history data available to undertake these analyses and fewer still have looked at the challenges to population viability posed by fragmentation—a feature inherent in agricultural landscapes where the matrix is highly modified. Our aim was to investigate the population viability of a large burrowing frog in an agricultural landscape. Specifically, we aimed to investigate the future persistence of populations under a range of scenarios including populations connected by various levels of dispersal and reduced rainfall. We used the life-history parameters of Heleioporus albopunctatus, a frog species widely distributed in the extensively cleared agricultural regions of south-western Australia. We investigated the viability of 24 partially connected populations under a range of scenarios using the program Vortex Version 10.1.6.0. Metapopulations were consistently more robust to extinction than isolated local populations. Both meta- and local populations were more susceptible to increases in age-specific mortality rates than to variation in the estimated ability of H. albopunctatus to disperse between breeding ponds, the survival rate of dispersers, or the frequency of drought. Our results reinforce the importance of metapopulations for survival in fragmented landscapes and point to the need to manage amphibian breeding ponds across landscapes to ensure high survival rates, particularly for juveniles.