A metapopulation paradox: partial improvement of habitat may reduce metapopulation persistence

The adverse influence of habitat degradation on the survival of populations may sometimes be amplified by rapid evolution over ecological timescales. This phenomenon of "evolutionary suicide" has been described in theoretical as well as empirical studies. However, no studies have suggested that habitat improvement could possibly also trigger an evolutionary response that would result in a decline in population size. We use individual-based simulations to demonstrate the potential for such a paradoxical response. An increase in the quality, size, or stability of only a fraction of the habitat patches in a metapopulation may result in an evolutionary decline in the dispersal propensity of individuals, followed by a decrease in recolonization, a reduction in the number of patches occupied, a decline in overall population size, and even extinction. Thus, well-intended conservation efforts that ignore potential evolutionary consequences of habitat management may increase the extinction risk of populations.     

Measuring dispersal in a metapopulation using stable isotope enrichment: high rates of sex-biased dispersal between patches in a mayfly metapopulation

Dispersal affects a wide array of ecological and evolutionary processes, but has been difficult to estimate empirically. A ¹⁵Nitrogen stable isotope enrichment technique was used to passively mark all developing Callibaetis ferrugineus hageni (Eaton) mayfly larvae in a beaver pond that had previously been shown to be a patch in a source-sink metapopulation. After enrichment during the larval stages, dispersal among ponds by adult females was demonstrated by the presence of unmarked females ovipositing in the labeled pond, and marked females in an unlabeled pond. Observed frequencies of marked females suggested incomplete mixing between ponds. In contrast, males rarely dispersed from their natal pond, which was consistent with the unusual mating system in this species – adult Callibaetis are short-lived, do not feed, and females are sexually receptive immediately after emerging from the larval habitat. The frequent dispersal demonstrated using the stable isotope technique was a critical component of the source-sink dynamic observed in this metapopulation, and further use of this technique will provide insights into patterns of dispersal in spatially structured habitats.     

On valuing patches: estimating contributions to metapopulation growth with reverse-time capture-recapture modelling

Metapopulation ecology has historically been rich in theory, yet analytical approaches for inferring demographic relationships among local populations have been few. We show how reverse-time multi-state capture-recapture models can be used to estimate the importance of local recruitment and interpopulation dispersal to metapopulation growth. We use 'contribution metrics' to infer demographic connectedness among eight local populations of banner-tailed kangaroo rats, to assess their demographic closure, and to investigate sources of variation in these contributions. Using a 7 year dataset, we show that: (i) local populations are relatively independent demographically, and contributions to local population growth via dispersal within the system decline with distance; (ii) growth contributions via local survival and recruitment are greater for adults than juveniles, while contributions involving dispersal are greater for juveniles; (iii) central populations rely more on local recruitment and survival than peripheral populations; (iv) contributions involving dispersal are not clearly related to overall metapopulation density; and (v) estimated contributions from outside the system are unexpectedly large. Our analytical framework can classify metapopulations on a continuum between demographic independence and panmixia, detect hidden population growth contributions, and make inference about other population linkage forms, including rescue effects and source-sink structures. Finally, we discuss differences between demographic and genetic population linkage patterns for our system.     

Conserving critical sites for biodiversity provides disproportionate benefits to people

Protecting natural habitats in priority areas is essential to halt the loss of biodiversity. Yet whether these benefits for biodiversity also yield benefits for human well-being remains controversial. Here we assess the potential human well-being benefits of safeguarding a global network of sites identified as top priorities for the conservation of threatened species. Conserving these sites would yield benefits--in terms of a) climate change mitigation through avoidance of CO(2) emissions from deforestation; b) freshwater services to downstream human populations; c) retention of option value; and d) benefits to maintenance of human cultural diversity--significantly exceeding those anticipated from randomly selected sites within the same countries and ecoregions. Results suggest that safeguarding sites important for biodiversity conservation provides substantial benefits to human well-being.     

Analysis of genetic diversity in a peatland specialist butterfly suggests an important role for habitat quality and small habitat patches

Understanding effects of habitat and landscape features on genetic variation is a prerequisite for the development of habitat and landscape management strategies aimed at conserving genetic diversity. While there has been considerable research on the effects of landscape structure on the genetics of populations, a recent review identified key biases in this body of work. The majority of landscape genetic studies investigate the intervening matrix’s influence on differentiation and gene flow among populations. Although characteristics of local habitat patches may be important determinants of genetic diversity, fewer studies have examined these relationships. Here we use node- and neighbourhood-based approaches to analyze correlates of genetic diversity in the bog copper (Lycaena epixanthe), a specialist butterfly endemic to temperate Nearctic peatlands that is threatened in parts of its range. Based on 190 repeatable and polymorphic amplified fragment length polymorphism loci, we found that genetic diversity was higher in habitat patches that were smaller and surrounded by more open water. Our results indicate that valuing small peatlands and preserving the surrounding water table may be important for conservation of genetic diversity in this highly specialized species. Our study highlights the importance of variables affecting habitat quality for conservation genetics.     

Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach

Temperature increases because of climate change are expected to cause expansions at the high latitude margins of species distributions, but, in practice, fragmented landscapes act as barriers to colonization for most species. Understanding how species distributions will shift in response to climate change therefore requires techniques that incorporate the combined effects of climate and landscape‐scale habitat availability on colonization rates. We use a metapopulation model (Incidence Function Model, IFM) to test effects of fine‐scale habitat use on patterns and rates of range expansion by the butterfly Hesperia comma. At its northern range margin in Britain, this species has increased its breadth of microhabitat use because of climate warming, leading to increased colonization rates. We validated the IFM by reconstructing expansions in five habitat networks between 1982 and 2000, before using it to predict metapopulation dynamics over 100 yr, for three scenarios based on observed changes to habitat use. We define the scenarios as “cold‐world” (only hot, south‐facing 150–250° hillsides are deemed warm enough), “warm‐world” in which 100–300° hillsides can be populated, and “hot‐world”, where the background climate is warm enough to enable use of all aspects (as increasingly observed). In the simulations, increased habitat availability in the hot‐world scenario led to faster range expansion rates, and to long‐term differences in distribution size and pattern. Thus, fine‐scale changes in the distribution of suitable microclimates led to landscape‐scale changes in population size and colonization rate, resulting in coarse‐scale changes to the species distribution. Despite use of a wider range of habitats associated with climate change, H. comma is still expected to occupy a small fraction of available habitat in 100 yr. The research shows that metapopulation models represent a potential framework to identify barriers to range expansion, and to predict the effects of environmental change or conservation interventions on species distributions and persistence.     

Patchy populations in stochastic environments: critical number of patches for persistence

We introduce a model for the dynamics of a patchy population in a stochastic environment and derive a criterion for its persistence. This criterion is based on the geometric mean (GM) through time of the spatial-arithmetic mean of growth rates. For the population to persist, the GM has to be >/=1. The GM increases with the number of patches (because the sampling error is reduced) and decreases with both the variance and the spatial covariance of growth rates. We derive analytical expressions for the minimum number of patches (and the maximum harvesting rate) required for the persistence of the population. As the magnitude of environmental fluctuations increases, the number of patches required for persistence increases, and the fraction of individuals that can be harvested decreases. The novelty of our approach is that we focus on Malthusian local population dynamics with high dispersal and strong environmental variability from year to year. Unlike previous models of patchy populations that assume an infinite number of patches, we focus specifically on the effect that the number of patches has on population persistence. Our work is therefore directly relevant to patchily distributed organisms that are restricted to a small number of habitat patches.     

Node self‐connections and metapopulation persistence: reply to Saura (2018)

Saura ( 2018 ) claims that studies using the Probability of Connectivity metric (PC) had already demonstrated the importance of including node self‐connections in network metrics. As originally defined and used, PC cannot test the importance of self‐connections. However, with key terms redefined, PC could be a useful tool in future work.     

Local population persistence as a pre-condition for large-scale dispersal of Idotea metallica(Crustacea, Isopoda) on drifting habitat patches

Idotea metallica establishes self-sustaining populations exclusively on objects drifting at the sea surface. Large-scale transport of drift material with surface currents results in an efficient dispersal of the species. Two types of drifting objects are utilised (biotic and abiotic), providing quite different conditions of life. Ephemeral biotic substrata (mainly uprooted macroalgae) may be used for transport and food, however, resulting habitat destruction from feeding must be a major threat for local population persistence of I. metallica. Abiotic substrata or wood represent efficient vectors for long-distance dispersal due to their resistance to biodegradation, but do not provide food for this herbivorous species. In laboratory experiments, the spatially-limited conditions of drifting substrata were simulated in microcosms. Idotea metallica established persistent populations on both types of substrata. On abiotic substrata, however, where the animals were fed only on Artemia larvae, high variations in density and a reduced intrinsic rate of population growth increased the risk of population extinction. Idotea metallica avoids habitat destruction by limited feeding on macroalgae. In contrast, the coastally distributed congener Idotea baltica destroyed algal habitats by feeding about 10 times faster than I. metallica.     

Multi-node selection of patches for protecting habitat connectivity: Fragmentation versus reachability

Landscape connectivity is of major importance in biodiversity conservation, and is one of the key aspects to be taken into consideration in the spatial design of networks of protected areas. Graph-theoretical approaches are useful in modelling habitat connectivity and defining priority areas for the protection of connectivity. This prioritization can be done based on rankings of the centrality (or importance) of individual habitat patches. Moreover, the centrality of a set of n habitat patches can also be calculated. Importantly, the most central single patch is not necessarily a member of the most central group of n patches (non-nested topology). Multi-node analyses identify groups of patches that maximally complement each other in order to increase the protection of connectivity for the whole network. We apply multi-node analyses to the prioritization of habitat patches for five vulnerable bird species in Catalonia, Spain, using two different approaches to connectivity, based on fragmentation and reachability. Groups of patches based on fragmentation are usually concentrated in core areas, while reachability groups are widely spread. Fragmentation sets have higher centrality value for low-mobility species, and reachability sets for long distance dispersers. The protection of the networks against fragmentation requires fewer patches, allows for more gradual implementation and is currently better accounted for by the Natura 2000 network of protected areas, while the protection of reachability is less costly and more efficient in terms of area requirements. Our work contributes to the development of landscape graph analysis for reserve design towards multi-node approaches.     

An easy-to-use index of ecological integrity for prioritizing freshwater sites and for assessing habitat quality

Prioritizing and assessing the condition of sites for conservation action requires robust and ergonomic methodological tools. We focus here on prioritizing freshwater sites using two promising biodiversity indices, the Dragonfly Biotic Index (DBI) and Average Taxonomic Distinctness (AvTD). The AvTD had no significant association with either species richness or endemism. In contrast, the DBI was highly significantly associated with species richness and endemism, although the strengths of the associations were weak. These associations are related to how the sub-indices in the DBI are weighted, and how species are distributed geographically. Additionally, the DBI was found to be very useful for site selection based on its ability to measure ecological integrity, combined with level of threat, at multiple spatial scales. The AvTD was found to be useful principally for regional use. As the DBI is a low-cost, easy-to-use method, it has the additional use as a method for assessing habitat quality and recovery in restoration programs. The DBI operates at the species level, and is therefore highly sensitive to habitat condition and has great potential for environmental assessment and monitoring freshwater biodiversity and quality. Practical, worked examples of river restoration are given here. In view of the ease and versatility by which the DBI can be employed, we recommend its testing and possible integration into freshwater management and conservation schemes elsewhere in the world.     

Contribution of habitat patches to network connectivity: Redundancy and uniqueness of topological indices

In order to increase the efficiency of monitoring and conservation efforts, it is of key importance to develop sound quantitative methods that are able to indicate which key areas and landscape elements play prominent and crucial role in the functioning of habitat mosaics. In particular, network models are being widely used to evaluate the contribution of landscape elements to uphold connectivity and related ecological fluxes. However, monitoring programs and conservation practitioners are overwhelmed by a myriad of network indices without being fully aware of their differences for characterizing the importance of individual habitat patches in fragmented landscapes. We analysed a set of thirteen commonly used graph indices and the forest habitat network of goshawks living in NE Spain in order to (a) evaluate how the patch rank orders derived from these indices differ from each other and (b) identify which indices tend to quantify the same network characteristics and which others are quite unique in addressing topological characteristics that are not considered by the rest. We found that most of the variability in patch rankings can be captured by only three network indices. The largest group of redundant indices corresponded to those that intend to measure the amount of flux received by a given habitat patch. The connector fraction of the integral index of connectivity (IIC) and probability of connectivity (PC) indices and betweenness centrality (BC) stood out as quite unique by focusing on the way habitat patches act as connecting elements between other habitat areas. We discuss which indices can be most beneficial by clearly indicating and differentiating the value of the top patches compared to the others, so that conservation priorities can be established with lower uncertainties. We believe that our results can provide valuable guidelines by facilitating the selection of a few non-redundant and complementary indicators that quantify the important and distinctive roles of habitat patches in maintaining the connectivity of habitat networks.     

The relative contribution of local habitat and landscape context to metapopulation processes: a dynamic occupancy modeling approach

Changes in site occupancy across habitat patches have often been attributed to landscape features in fragmented systems, particularly when considering metapopulations. However, failure to include habitat quality of individual patches can mask the relative importance of local scale features in determining distributional changes. We employed dynamic occupancy modeling to compare the strength of local habitat variables and metrics of landscape patterns as drivers of metapopulation dynamics for a vulnerable, high‐elevation species in a naturally fragmented landscape. Repeat surveys of Bicknell's thrush Catharus bicknelli presence/non‐detection were conducted at 88 sites across Vermont, USA in 2006 and 2007. We used an organism‐based approach, such that at each site we measured important local‐scale habitat characteristics and quantified landscape‐scale features using a predictive habitat model for this species. We performed a principal component analysis on both the local and landscape features to reduce dimensionality. We estimated site occupancy, colonization, and extinction probabilities while accounting for imperfect detection. Univariate, additive, and interaction models of local habitat and landscape context were ranked using AICc scores. Both local and landscape scales were important in determining changes in occupancy patterns. An interaction between scales was detected for occupancy dynamics indicating that the relationship of the parameters to local‐scale habitat conditions can change depending on the landscape context and vice versa. An increase in both landscape‐ and local‐scale habitat quality increased occupancy and colonization probability while decreasing extinction risk. Colonization and extinction were both more strongly influenced by local habitat quality relative to landscape patterns. We also identified clear, qualitative thresholds for landscape‐scale features. Conservation of large habitat patches in high‐cover landscapes will help ensure persistence of Bicknell's thrushes, but only if local scale habitat quality is maintained. Our results highlight the importance of incorporating information beyond landscape characteristics when investigating patch occupancy patterns in metapopulations.     

Butterfly abundance and movements among prairie patches: the roles of habitat quality, edge, and forest matrix permeability

The spatial distribution of patchy insect populations is partly caused by behavioral patterns of insect movement that are influenced by habitat quality, isolation, and the permeability of the surrounding matrix. We recorded insect movements, abundance, and edge behaviors in two species of butterflies, the great-spangled fritillary (Speyeria cybele F., Lepidoptera: Nymphalidae) and the pearl crescent (Phyciodes tharos Drury, Lepidoptera: Nymphalidae), inhabiting remnant prairies surrounded by a forest matrix in south-central Ohio. We also determined the number of forest matrix types present and recorded the permeability of the different types to butterfly movement. The great-spangled fritillary exhibited a relatively high number of interpatch movements, a higher abundance at patch edges, and a propensity to cross the prairie-forest edges, and the forest matrix had a high permeability to butterfly movement. The pearl crescent, in contrast, rarely crossed edge boundaries, moved infrequently among patches, and was more abundant within the patch interior and in patches with high host-plant and flower densities. There were three structurally different forest matrix types separating habitat patches, which in previous studies would have been classified as a single deciduous forest matrix. Butterfly movement and edge behaviors mechanistically interact with patch quality, isolation, and the matrix permeability to determine the spatial structure of these populations in fragmented habitats.     

Single large AND several small habitat patches: A community perspective on their importance for biodiversity

The debate whether single large or several small (SLOSS) patches benefit biodiversity has existed for decades, but recent literature provides increasing evidence for the importance of small habitats. Possible beneficial mechanisms include reduced presence of predators and competitors in small habitat areas or specific functions such as stepping stones for dispersal. Given the increasing amount of studies highlighting individual behavioral differences that may influence these functions, we hypothesize that the advantage of small versus large habitat patches not only depends on patch functionality but also on the presence of animal personalities (i.e., risk-tolerant vs. risk-averse). Using an individual-based, spatially-explicit community model, we analyzed the diversity of mammal communities in landscapes consisting of a few large habitat islands interspersed with different amounts and sizes of small habitat patches. Within these heterogeneous environments, individuals compete for resources and form home-ranges, with only risk-tolerant individuals using habitat edges. Results show that when risk-tolerant individuals exist, small patches increase species diversity. A strong peak occurs at approximately 20% habitat cover in small patches when those small habitats are only used for foraging but not for breeding and home-range core position. Additional usage as stepping stones for juvenile dispersal further increases species persistence. Overall, our results reveal that a combination of a few large and several small habitat patches promotes biodiversity by enhancing landscape heterogeneity. Here, heterogeneity is created by pronounced differences in habitat functionality, increasing edge density, and variability in habitat use by different behavioral types. The finding that a combination of single large AND several small (SLASS) patches is needed for effective biodiversity preservation has implications for advancing landscape conservation. Particularly in structurally poor agricultural areas, modern technology enables precise management with the opportunity to create small foraging habitats by excluding less profitable agricultural land from cultivation.