Using connectivity metrics in conservation planning – when does habitat quality matter?

Aim The objective of conservation planning is often to prioritize patches based on their estimated contribution to metapopulation or metacommunity viability. The contribution that an individual patch makes will depend on its intrinsic characteristics, such as habitat quality, as well as its location relative to other patches, its connectivity. Here we systematically evaluate five patch value metrics to determine the importance of including an estimate of habitat quality into the metrics. Location We tested the metrics in landscapes designed to represent different degrees of variability in patch quality and different levels of patch aggregation. Methods In each landscape, we simulated population dynamics using a spatially explicit, continuous time metapopulation model linked to within patch logistic growth models. We tested five metrics that are used to estimate the contribution that a patch makes to metapopulation viability: two versions of the probability of connectivity index, two versions of patch centrality (a graph theory metric) and the metapopulation capacity metric. Results All metrics performed best in environments where patch quality was very variable and high quality patches were aggregated. Metrics that incorporated some measure of patch quality did better in all environments, but did particularly well in environments with high variance of patch quality and spatial aggregation of good quality patches. Main conclusions Including an estimate of patch quality significantly increased the ability of a given connectivity metric to rank correctly habitat patches according to their contribution to metapopulation viability. Incorporating patch quality is particularly important in landscapes where habitat quality is highly variable and good quality patches are spatially aggregated. However, caution should be used when applying patch metrics to homogeneous landscapes, even if good estimates of patch quality are available. Our results demonstrate that landscape structure and the degree of variability in patch quality need to be assessed prior to selecting a suitable method for estimating patch value.     

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.     

Effect of habitat fragmentation on dispersal in the butterfly Proclossiana eunomia

Comparison of dispersal rates of the bog fritillary butterfly between continuous and fragmented landscapes indicates that between patch dispersal is significantly lower in the fragmented landscape, while population densities are of the same order of magnitude. Analyses of the dynamics of the suitable habitat for the butterfly in the fragmented landscape reveal a severe, non linear increase in spatial isolation of patches over a time period of 30 years (i.e. 30 butterfly generations), but simulations of the butterfly metapopulation dynamics using a structured population model show that the lower dispersal rates in the fragmented landscape are far above the critical threshold leading to metapopulation extinction. These results indicate that changes in individual behaviour leading to the decrease of dispersal rates in the fragmented landscape were rapidly selected for when patch spatial isolation increased. The evidence of such an adaptive answer to habitat fragmentation suggests that dispersal mortality is a key factor for metapopulation persistence in fragmented landscapes. We emphasise that landscape spatial configuration and patch isolation have to be taken into account in the debate about large-scale conservation strategies.     

Connectivity conservation priorities for individual patches evaluated in the present landscape: how durable and effective are they in the long term?

One of the most widespread approaches for setting spatially‐explicit priorities for connectivity conservation consists in evaluating the effects of the individual removal of each habitat patch (one at a time) from the landscape. It however remains unknown the degree to which such priorities are valid and reliable in the longer term, as subsequent habitat losses and other disruptions accumulate in the landscape. We compared the patch prioritizations and estimated connectivity losses resulting from individual patch removals and from a more exhaustive assessment accounting for the potentially synergistic impacts of multiple habitat losses by testing all possible combinations of patch removals. Habitat availability (reachability) metrics and metapopulation capacity were calculated in purposefully simulated landscapes and in habitat distribution data for three bird species (NE Spain). We found that 1) individual patch removals allowed identifying areas of low contribution to connectivity that remained so after subsequent network modifications, 2) the most important patches identified through individual removals often did not coincide with those patches whose removal would actually be most detrimental after multiple habitat losses. However, these differences were smaller for the habitat reachability metrics, as well as for very mobile species that were largely insensitive to habitat spatial arrangement. If many patch losses over time are likely, it might be a more robust and fruitful conservation strategy for managers to pinpoint those patches that, with a low negative impact on connectivity, can be converted to other land uses, instead of trying to elucidate through individual patch removals which subset of protected patches would be the most effective for conserving as much connectivity as possible in the long term. Individual patch removals provide useful but non‐permanent guidelines that may need to be reassessed when substantial landscape modifications occur, which requires dynamic strategies for connectivity conservation in the face of global change.     

Emergent properties of conspecific attraction in fragmented landscapes

Attraction to conspecifics may have wide-ranging implications for habitat selection and metapopulation theory, yet little is known about the process of attraction and its effects relative to other habitat selection strategies. Using individual-based simulations, I investigated the emergent properties of conspecific attraction during habitat selection on survival, fecundity, short-term fitness (survival x fecundity), and distributions in fragmented landscapes. I simulated conspecific attraction during searching and settlement decisions and compared attraction with random, habitat-based (searching for the presence of habitat), and habitat quality sampling strategies (searching for and settling in high-quality habitat). Conspecific attraction during searching or settlement decisions had different consequences for animals: attraction while searching increased survival by decreasing time spent in nonsuitable habitat, whereas attraction during settlement increased fecundity by aggregating animals in high-quality habitats. Habitat-based sampling did not improve fitness over attraction, but directly sampling habitat quality resulted in the highest short-term fitness among strategies. These results suggest that attraction can improve fitness when animals cannot directly assess habitat quality. Interestingly, conspecific attraction influenced distributions by generating patch size effects and weak edge effects, highlighting that attraction is one potential, yet previously unappreciated, mechanism to explain the widespread patterns of animal sensitivity to habitat fragmentation.     

Adaptive walks on behavioural landscapes and the evolution of optimal behaviour by natural selection

Summary One of the main challenges to the adaptationist programme in general and to the use of optimality models in behavioural and evolutionary ecology in particular is that natural selection need not optimise fitness. This challenge is addressed by considering the evolution of optimal patch choice by natural selection. The behavioural model is based on a state variable approach in which a strategy consists of a sequence denoting the patch to be visited as a function of the organism's state and time. The optimal strategy maximises expected terminal reproduction. The fitnesses of alternative strategies are computed by iteration of the associated equations for fitness; this characterises the adaptive behavioural landscape. There may be enormous numbers of strategies that have near optimal fitnesses. A population model is used to connect frequencies of behavioural types from one generation to the next. Theories on adaptive walks on fitness landscapes are considered in the context of behaviour. The main result is that within the context of optimality arguments at selective equilibrium, sub-optimal behaviours can persist. General implications for research in behavioural ecology, including tests of behavioural theories, are discussed.     

The evolution of an 'intelligent' dispersal strategy: biased, correlated random walks in patchy landscapes

Theoretical work exploring dispersal evolution focuses on the emigration rate of individuals and typically assumes that movement occurs either at random to any other patch or to one of the nearest‐neighbour patches. There is a lack of work exploring the process by which individuals move between patches, and how this process evolves. This is of concern because any organism that can exert control over dispersal direction can potentially evolve efficiencies in locating patches, and the process by which individuals find new patches will potentially have major effects on metapopulation dynamics and gene flow. Here, we take an initial step towards filling this knowledge gap. To do this we constructed a continuous space population model, in which individuals each carry heritable trait values that specify the characteristics of the biased correlated random walk they use to disperse from their natal patch. We explore how the evolution of the random walk depends upon the cost of dispersal, the density of patches in the landscape, and the emigration rate. The clearest result is that highly correlated walks always evolved (individuals tended to disperse in relatively straight lines from their natal patch), reflecting the efficiency of straight‐line movement. In our models, more costly dispersal resulted in walks with higher correlation between successive steps. However, the exact walk that evolved also depended upon the density of suitable habitat patches, with low density habitat evolving more biased walks (individuals which orient towards suitable habitat at quite large distances from that habitat). Thus, low density habitat will tend to develop individuals which disperse efficiently between adjacent habitat patches but which only rarely disperse to more distant patches; a result that has clear implications for metapopulation theory. Hence, an understanding of the movement behaviour of dispersing individuals is critical for robust long‐term predictions of population dynamics in fragmented landscapes.     

Toward ecologically scaled landscape indices

Nature conservation is increasingly based on a landscape approach rather than a species approach. Landscape planning that includes nature conservation goals requires integrated ecological tools. However, species differ widely in their response to landscape change. We propose a framework of ecologically scaled landscape indices that takes into account this variation. Our approach is based on a combination of field studies of spatially structured populations (metapopulations) and model simulations in artificial landscapes. From these, we seek generalities in the relationship among species features, landscape indices, and metapopulation viability. The concept of ecological species profiles is used to group species according to characteristics that are important in metapopulations' response to landscape change: individual area requirements as the dominant characteristic of extinction risk in landscape patches and dispersal distance as the main determinant of the ability to colonize patches. The ecological profiles and landscape indices are then integrated into two ecologically scaled landscape indices (ESLI): average patch carrying capacity and average patch connectivity. The field data show that the fraction of occupied habitat patches is correlated with the two ESLI. To put the ESLI into a perspective of metapopulation persistence, we determine the viability for six ecological profiles at different degrees of habitat fragmentation using a metapopulation model and computer-generated landscapes. The model results show that the fraction of occupied patches is a good indicator for metapopulation viability. We discuss how ecological profiles, ESLI, and the viability threshold can be applied for landscape planning and design in nature conservation.     

Effects of aerial dispersal, habitat specialisation, and landscape structure on spider distribution across fragmented grey dunes

Species distribution patterns have been explained by Hutchinson's niche theory, metapopulation theory and source-sink theory. Empirical verification of this framework, however, remains surprisingly scant. In this paper, we test the hypothesis that landscape characteristics (patch size and connectivity), aerial dispersal ability and niche breadth interact in explaining distribution patterns of 29 spider species inhabiting fragmented grey dunes. Distribution patterns only depended on aerial dispersal potential, and the interaction between patch connectivity and area. Niche breadth, measured as the degree of habitat specialisation in the total coastal dune system, did not contribute to the observed distribution patterns. Additional variation in patch occupancy frequency was strongly species-dependent and was determined by different responses to the degree of patch connectivity for ballooning dispersal. Results from this study suggest that dispersal ability largely affects our perception of a species "fundamental niche", and that source-sink and metapopulation dynamics may have a major impact on the distribution of species. From a conservation point of view, specialised (and hence intrinsically rare) species can be predicted to become rarer if fragmentation increases and connectivity decreases. This study is, to our knowledge, one of the few linking species distribution (and not patch occupancy, species diversity or richness) to landscape ecological (patch connectivity and area) and auto-ecological (niche breadth, dispersal potential) features.     

Agent-based model approach to optimal foraging in heterogeneous landscapes: effects of patch clumpiness

Optimal foraging theory concerns animal behavior in landscapes where food is concentrated in patches. The efficiency of foraging is an effect of both the animal behavior and the geometry of the landscape; furthermore, the landscape is itself affected by the foraging of animals. We investigated the effect of landscape heterogeneity on the efficiency of an optimal forager. The particular aspect of heterogeneity we considered was "clumpiness"– the degree to which food resource patches are clustered together. The starting point for our study was the framework of the Mean Value Theorem (MVT) by Charnov. Since MVT is not spatially explicit, and thus not apt to investigate effects of clumpiness, we built an agent-based (or individual-based) model for animal movement in discrete landscapes extending the MVT. We also constructed a model for generating landscapes where the clumpiness of patches can be easily controlled, or "tuned", by an input parameter. We evaluated the agent based model by comparing the results with what the MTV would give, i.e. if the spatial effects were removed. The MVT matched the simulations best on landscapes with random patch configuration and high food recovery rates. As for our main question about the effects of clumpiness, we found that, when landscapes were highly productive (rapid food replenishment), foraging efficiency was greatest in clumped landscapes. In less productive landscapes, however, foraging efficiency was lowest in landscapes with a clumped patch distribution.     

Can the assumption of a non‐random search improve our prediction of butterfly fluxes between resource patches?

Abstract. 1. Understanding dispersal patterns that enable small, spatially isolated populations to survive in fragmented landscapes has become an important issue in conservation biology and landscape management. However, for most of the species of interest it is not known whether dispersing individuals navigate or follow systematic search strategies, as opposed to moving randomly. 2. Recently it was shown that individuals of the butterfly species Maniola jurtina do not seek resources by means of random flight. If true, this may be problematic for existing metapopulation models, including those based on the evolution of dispersal rates in metapopulations. 3. The study tested to what extent the non‐random dispersal patterns described in the literature can explain M. jurtina fluxes in its natural habitat. 4. A model based on literature assumptions of M. jurtina movements is presented in the work reported here, and its predictions are compared with 2 years of capture–recapture data on its fluxes in two landscapes. 5. The model provides a good fit to the data and gives better predictions than the model based only on patch sizes and distances between patches. 6. Thus, if data are available about the actual landscape under consideration, the model should be preferred to simpler approaches; however, in general theoretical considerations the simple approach based on patch size and the degree of its isolation will retain its value.     

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.     

Spatial occurrence and colonisations in patch-tracking metapopulations: local conditions versus dispersal

We studied the relative importance of local variables and dispersal for the occurrence and colonisation of the epiphytic bryophytes Orthotricum speciosum (spore dispersed), and O. obtusifolium (spore and asexual gemmae) on aspen trees ('patches') in two forest landscapes (one old-growth and one fragmented) using multiple logistic regression. The relative importance of dispersal was quantified as the reduction of residual deviance for a connectivity variable. In modelling dispersal, we assumed that trees with low local abundance were recent colonisations, and that trees with high local abundance were diaspore sources for colonisation. The occurrence of O. speciosum in the fragmented landscape was most affected by shading, but also by connectivity, aspen diameter and vitality. In the old-growth landscape, connectivity was the single most important variable for recent colonisations, but its effect was lower than the sum of the effects of all local environmental variables. The occurrence of O. obtusifolium in the fragmented landscape was related to similar variables but the relative importance of these variables was different, and connectivity did not affect the probability of a recent colonisation in this species. We describe the epiphyte-tree system in the patch-tracking metapopulation model. In this model colonisations are distance dependent, but in contrast to the classical metapopulation model local extinctions are caused by deterministic patch destruction – once the epiphyte has colonised the tree it remains until the tree dies.     

Metapopulation persistence in dynamic landscapes: the role of dispersal distance

Species associated with transient habitats need efficient dispersal strategies to ensure their regional survival. Using a spatially explicit metapopulation model, we studied the effect of the dispersal range on the persistence of a metapopulation as a function of the local population and landscape dynamics (including habitat patch destruction and subsequent regeneration). Our results show that the impact of the dispersal range depends on both the local population and patch growth. This is due to interactions between dispersal and the dynamics of patches and populations via the number of potential dispersers. In general, long-range dispersal had a positive effect on persistence in a dynamic landscape compared to short-range dispersal. Long-range dispersal increases the number of couplings between the patches and thus the colonisation of regenerated patches. However, long-range dispersal lost its advantage for long-term persistence when the number of potential dispersers was low due to small population growth rates and/or small patch growth rates. Its advantage also disappeared with complex local population dynamics and in a landscape with clumped patch distribution.     

Modelling the spatial dynamics and persistence of the leaf beetle Gonioctena olivacea in dynamic habitats

In dynamic landscapes natural and anthropogenic disturbance as well as succession are responsible for the emergence and subsequent disappearance of suitable habitat patches. Species inhabiting such landscapes are faced with varying number and spatial configuration of patches. A stochastic, spatially explicit simulation model was developed in order to analyse the persistence of the leaf beetle Gonioctena olivacea in a system of dynamic patches of its host plant Cytisus scoparius . The model was parameterized with data from a three-year field study on the spatial configuration, distribution, and turnover of the host plant patches as well as the patch occupancy, extinction, and colonization rates of the beetle. The simulations showed large fluctuations in the occurrence of the beetle in the patches. High levels of occupancy were related to high aggregation of the patches within the landscape. The velocity of patch turnover was found to have a severe effect on the persistence of the beetle metapopulation. Enhancing the turnover rate by only a few patches, the mean time to extinction decreases rapidly. Moreover, the results revealed that not necessarily an effect of connectivity can be detected in the analysis of occupancy patterns in dynamic landscapes, although the colonization of patches is clearly connectivity-dependent. In general, this modelling study demonstrates the importance of detailed information on patch turnover. The amount and spatial distribution of suitable habitat is a major driver of metapopulation dynamics of species in dynamic landscapes.     

An integrative framework of coexistence mechanisms in competitive metacommunities

Species distribution in a metacommunity varies according to their traits, the distribution of environmental conditions and connectivity among localities. These ingredients contribute to coexistence across spatial scales via species sorting, patch dynamics, mass effects and neutral dynamics. These mechanisms however seldom act in isolation and the impact of landscape configuration on their relative importance remains poorly understood. We present a new model of metacommunity dynamics that simultaneously considers these four possible mechanisms over spatially explicit landscapes and propose a statistical approach to partition their contribution to species distribution. We find that landscape configuration can induce dispersal limitations that have negative consequences for local species richness. This result was more pronounced with neutral dynamics and mass effect than with species sorting or patch dynamics. We also find that the relative importance of the four mechanisms varies not only among landscape configurations, but also among species, with some species being mostly constrained by dispersal and/or drift and others by sorting. Changes in landscape properties might lead to a shift in coexistence mechanisms and, by extension, to a change in community composition. This confirms the importance of considering landscape properties for conservation and management. Our results illustrate the idea that ecological communities are the results of multiple mechanisms acting at the same time and complete our understanding of spatial processes in competitive metacommunities.     

Modularity along organism dispersal gradients challenges a prevailing view of abrupt transitions in animal landscape perception

A common property of landscapes and metacommunities is the occurrence of abrupt shifts in connectivity along gradients of individual dispersal abilities. Animals with short‐range dispersal capability perceive fragmented landscapes, but organisms moving across critical thresholds perceive continuous landscapes. This qualitative shift in landscape perception may determine several attributes of local communities and the dynamics of whole metacommunities. Modularity describes the existence in some communities of relatively high numbers of mutual connections favoring the movement of neighboring individuals (even when each individual is able to reach any patch in the landscape). Local patch linkages and metacommunity connectivity along gradients of dispersal ability have been reported frequently. However, the intermediate level of structure captured by modularity has not been considered. We evaluated landscape connectivity and modularity along gradients of individual dispersal abilities. Random landscapes with different degrees of cell aggregation and occupancy were simulated; we also analyzed ten real ecosystems. An expected, a shift in landscape connectivity was always detected; modularity consistently decreased gradually along dispersal gradients in both simulated networks and empirical landscapes. Neutral metacommunities within simulated landscapes demonstrated that modularity and connectivity may reflect landscape traits in the shaping of metacommunity diversity. Average beta‐diversity was strongly associated with modularity, particularly with low migration rates, while connectivity trends tracked changes in beta‐diversity at intermediate to high migrations rates. Consequently, while some species are able to perceive abrupt transitions in the landscape, many others probably experience a gradual continuum in landscape perception, contrary to predictions from previous analyses. Furthermore, the gradual behavior of modularity indicates that it may represent an exceptional early‐warning tool that measures system distance to tipping points. Our study highlights the multiple perceptions that different species may have of a single landscape and shows, for the first time, a theoretical and empirical relationship between landscape modularity, and metacommunity diversity.     

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.     

Vertically transmitted symbionts in structured host metapopulations

We develop a structured metapopulation model for vertically transmitted symbionts in natural host populations. We focus primarily on two questions: Are mutualism and high transmission probability prerequisites for the survival of symbionts in structured host metapopulations? What are the ecological conditions under which coexistence of infected and uninfected hosts is possible? We start with studying in depth the case of qualitatively identical patches and derive conditions for invasion and coexistence of uninfected and infected hosts. Our model predicts that, in a qualitatively uniform environment, coexistence is possible only if the symbionts increase the fitness of their host, so the mutualism is indeed needed for coexistence. We also prove that evolution selects for 100% infection frequency in the metapopulation. Then we generalize the model for different patch qualities and get conditions for invasion in a virgin environment.     

Variation in migration propensity among individuals maintained by landscape structure

Metapopulation dynamics lead to predictable patterns of habitat occupancy, population density and trophic structure in relation to landscape features such as habitat patch size and isolation. Comparable patterns may occur in behavioural, physiological and life‐history traits but remain little studied. In the Glanville fritillary butterfly, females in newly established populations were more mobile than females in old populations. Among females from new populations, mobility decreased with increasing connectivity (decreasing isolation), but in females from old populations mobility increased with connectivity. The [ATP]/[ADP] ratio of flight muscles following controlled activity showed the same pattern as mobility in relation to population age and connectivity, suggesting that physiological differences in flight metabolic performance contribute to the observed variation in mobility. We demonstrate with an evolutionary metapopulation model parameterised for the Glanville fritillary that increasing spatial variation in landscape structure increases variance in mobility among individuals in a metapopulation, supporting the general notion that complex landscape structure maintains life‐history variation.