Nicolas Schtickzelle

Costs of dispersal

Dispersal costs can be classified into energetic, time, risk and opportunity costs and may be levied directly or deferred during departure, transfer and settlement. They may equally be incurred during life stages before the actual dispersal event through investments in special morphologies. Because costs will eventually determine the performance of dispersing individuals and the evolution of dispersal, we here provide an extensive review on the different cost types that occur during dispersal in a wide array of organisms, ranging from micro‐organisms to plants, invertebrates and vertebrates. In general, costs of transfer have been more widely documented in actively dispersing organisms, in contrast to a greater focus on costs during departure and settlement in plants and animals with a passive transfer phase. Costs related to the development of specific dispersal attributes appear to be much more prominent than previously accepted. Because costs induce trade‐offs, they give rise to covariation between dispersal and other life‐history traits at different scales of organismal organisation. The consequences of (i) the presence and magnitude of different costs during different phases of the dispersal process, and (ii) their internal organisation through covariation with other life‐history traits, are synthesised with respect to potential consequences for species conservation and the need for development of a new generation of spatial simulation models.

Behavioural responses to habitat patch boundaries restrict dispersal and generate emigration-patch area relationships in fragmented landscapes

We studied the consequences of behaviour at habitat patch boundaries on dispersal for the bog fritillary butterfly Proclossiana eunomia Esper in two networks of habitat differing in fragmentation and matrix quality. We tested for differences in responses to patch boundaries according to the fragmentation level of the network by analysing movement paths of adult butterflies. Butterflies systematically engaged in U-turns when they reached a boundary in the fragmented network while they crossed over boundaries in more than 40% of boundary encounters in the continuous one. We applied the Virtual Migration model (Hanski, Alho & Moilanen 2000) to capture-mark-recapture data collected in both networks. The model indicated (i) a lower dispersal rate and (ii) a lower survival during dispersal in the fragmented network. This latter difference is likely to be the key biological process leading to behavioural avoidance of patch boundary crossings. On the basis of this behavioural difference, we designed an individual-based simulation model to explore the relationship between patch area, boundary permeability and emigration rate. Predictions of the model fitted observed results of the effect of patch area on emigration rate according to fragmentation: butterflies are more likely to leave small patches than large ones in fragmented landscapes (where patch boundary permeability is low), while this relationship disappears in more continuous landscapes (where patch boundary permeability is high).

DISPERSAL DEPRESSION WITH HABITAT FRAGMENTATION IN THE BOG FRITILLARY BUTTERFLY

Habitat fragmentation is expected to impose strong selective pressures on dispersal rates. However, evolutionary responses of dispersal are not self-evident, since various selection pressures act in opposite directions. Here we disentangled the components of dispersal behavior in a metapopulation context using the Virtual Migration model, and we linked their variation to habitat fragmentation in the specialist butterfly Proclossiana eunomia. Our study provided a nearly unique opportunity to study how habitat fragmentation modifies dispersal at the landscape scale, as opposed to microlandscapes or simulation studies. Indeed, we studied the same species in four landscapes with various habitat fragmentation levels, in which large amounts of field data were collected and analyzed using similar methodologies. We showed the existence of quantitative variations in dispersal behavior correlated with increased fragmentation. Dispersal propensity from habitat patches (for a given patch size), and mortality during dispersal (for a given patch connectivity) were lower in more fragmented landscapes. We suggest that these were the consequences of two different evolutionary responses of dispersal behavior at the individual level: (1) when fragmentation increased, the reluctance of individuals to cross habitat patch boundaries also increased; (2) when individuals dispersed, they flew straighter in the matrix, which is the best strategy to improve dispersal success. Such evolutionary responses could generate complex nonlinear patterns of dispersal changes at the metapopulation level according to habitat fragmentation. Due to the small size and increased isolation of habitat patches in fragmented landscapes, overall emigration rate and mortality during dispersal remained high. As a consequence, successful dispersal at the metapopulation scale remained limited. Therefore, to what extent the selection of individuals with a lower dispersal propensity and a higher survival during dispersal is able to limit detrimental effects of habitat fragmentation on dispersal success is unknown, and any conclusion that metapopulations would compensate for them is flawed.

Quantifying functional connectivity: experimental evidence for patch-specific resistance in the Natterjack toad (Bufo calamita)

Despite the importance assigned to inter-patch movements in fragmented systems, the structure of landscape between suitable habitat patches, the matrix, is often considered as to be of minor interest, or totally ignored. Consequently, models predicting metapopulation dynamics typically assume that dispersal and movement abilities are independent of the composition of the matrix. The predictions of such models should be invalided if that crucial assumption is unverified. In order to test the hypothesis of a patch-specific resistance, we led an experimental study to assess the matrix effects on the movement ability of juvenile Natterjack toads (Bufo calamita). The movement behaviour of first year toadlets, the dispersal stage in this species, was investigated in an arena experiment. Toadlet mobility was assessed in five landscape components that were mimicked in the lab: sandy soil, road, forest, agricultural field, and pasture. We analysed several movement components including move length, speed, efficiency and turning angle distribution. Our results showed that movement ability was strongly affected by the land cover, even if body size modulated the behavioural responses of toadlets. Performances were the best in the arenas mimicking sand and roads, and the worst in the forest arena, toadlet moves being three to five times less effective in the latter. The mobility was intermediate in the two other arenas. We propose here a new method to quantify functional connectivity, based on quantitative estimates of relative values for resistance of landscape components. This method offers a reliable alternative for resistance value estimates to subjective ‘expert advice’ or inference from genetic population structure.

Quantitative analysis of changes in movement behaviour within and outside habitat in a specialist butterfly

BackgroundDispersal between habitat patches is a key process in the functioning of (meta)populations. As distance between suitable habitats increases, the ongoing process of habitat fragmentation is expected to generate strong selection pressures on movement behaviour. This leads to an increase or decrease of dispersal according to its cost relative to landscape structure. To limit the cost of dispersal in an increasingly hostile matrix, we predict that organisms would adopt special dispersal behaviour between habitats, which are different from movements associated with resource searching in suitable habitats.ResultsHere we quantified the movement behaviour of the bog fritillary butterfly (Proclossiana eunomia) by (1) assessing perceptual range, the distance to which the habitat can be perceived, and (2) tracking and parameterizing movement behaviour within and outside habitat (parameters were move length and turning angles distributions). Results are three-fold. (1) Perceptual range was < 30 m. (2) Movements were significantly straighter in the matrix than within the habitat. (3) Correlated random walk adequately described movement behaviour for 70% of the observed movement paths within habitat and in the matrix.ConclusionThe perceptual range being lower than the distance between habitat patches in the study area, P. eunomia likely perceives these habitat networks as fragmented, and must locate suitable habitats while dispersing across the landscape matrix. Such a constraint means that dispersal entails costs, and that selection pressure should favour behaviours that limit these costs. Indeed, our finding that dispersal movements in the matrix are straighter than resource searching movements within habitat supports the prediction of simulation studies that adopting straight movements for dispersal reduces its costs in fragmented landscapes. Our results support the mounting evidence that dispersal in fragmented landscapes evolved towards the use of specific movement behaviour, different from explorative searching movements within habitat.

Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies

As ectothermic organisms, butterflies have widely been used as models to explore the predicted impacts of climate change. However, most studies explore only one life stage; to our best knowledge, none have integrated the impact of temperature on the vital rates of all life stages for a species of conservation concern. Besides, most population viability analysis models for butterflies are based on yearly population growth rate, precluding the implementation and assessment of important climate change scenarios, where climate change occurs mainly, or differently, during some seasons. Here, we used a combination of laboratory and field experiments to quantify the impact of temperature on all life stages of a vulnerable glacial relict butterfly. Next, we integrated these impacts into an overall population response using a deterministic periodic matrix model and explored the impact of several climate change scenarios. Temperature positively affected egg, pre-diapause larva and pupal survival, and the number of eggs laid by a female; only the survival of overwintering larva was negatively affected by an increase in temperature. Despite the positive impact of warming on many life stages, population viability was reduced under all scenarios, with predictions of much shorter times to extinction than under the baseline (current temperature situation) scenario. Indeed, model predictions were the most sensitive to changes in survival of overwintering larva, the only stage negatively affected by warming. A proper consideration of every stage of the life cycle is important when designing conservation guidelines in the light of climate change. This is in line with the resource-based habitat view, which explicitly refers to the habitat as a collection of resources needed for all life stages of the species. We, therefore, encourage adopting a resource-based habitat view for population viability analysis and development of conservation guidelines for butterflies, and more generally, other organisms. Life stages that are cryptic or difficult to study should not be forsaken as they may be key determinants in the overall response to climate change, as we found with overwintering Boloria eunomia larvae.

Positive correlation between genetic diversity and fitness in a large, well-connected metapopulation

BackgroundTheory predicts that lower dispersal, and associated gene flow, leads to decreased genetic diversity in small isolated populations, which generates adverse consequences for fitness, and subsequently for demography. Here we report for the first time this effect in a well-connected natural butterfly metapopulation with high population densities at the edge of its distribution range.ResultsWe demonstrate that: (1) lower genetic diversity was coupled to a sharp decrease in adult lifetime expectancy, a key component of individual fitness; (2) genetic diversity was positively correlated to the number of dispersing individuals (indicative of landscape functional connectivity) and adult population size; (3) parameters inferred from capture-recapture procedures (population size and dispersal events between patches) correlated much better with genetic diversity than estimates usually used as surrogates for population size (patch area and descriptors of habitat quality) and dispersal (structural connectivity index).ConclusionOur results suggest that dispersal is a very important factor maintaining genetic diversity. Even at a very local spatial scale in a metapopulation consisting of large high-density populations interconnected by considerable dispersal rates, genetic diversity can be decreased and directly affect the fitness of individuals. From a biodiversity conservation perspective, this study clearly shows the benefits of both in-depth demographic and genetic analyses. Accordingly, to ensure the long-term survival of populations, conservation actions should not be blindly based on patch area and structural isolation. This result may be especially pertinent for species at their range margins, particularly in this era of rapid environmental change.

Metapopulation dynamics of the bog fritillary butterfly: comparison of demographic parameters and dispersal between a continuous and a highly fragmented landscape

We investigated the effects of habitat loss and fragmentation on population functioning. We compared demography (daily and total population sizes) and dispersal (dispersal rate and dispersal kernels) of the bog fritillary butterfly in two 6-km2 landscapes differing in their degree of fragmentation. In 2000, we conducted a Capture-Mark-Recapture experiment in a highly fragmented system in the marginal part of the species distribution (Belgium) and in a more continuous system in the central part of its distribution (Finland). A total of 293 and 947 butterflies were marked with 286 and 190 recapture events recorded in the fragmented and the continuous system respectively. Our results suggest that habitat loss and fragmentation affect dispersal more than demography. Although density was lower in the continuous system, it remains in the yearly range of variation observed on 10 generations in the fragmented system. However, in the fragmented system, the dispersal rate dropped drastically (39 vs. 64%) and females moved longer distances. Patch area had a significant effect on migration in the fragmented system only. From our results, we propose the definition of a new parameter, the minimal patch area (MPA) needed to establish a local population in highly fragmented landscapes.

NEGATIVE RELATIONSHIP BETWEEN DISPERSAL DISTANCE AND DEMOGRAPHY IN BUTTERFLY METAPOPULATIONS

Little is known about the connection between demography and dispersal in metapopulations. The meta-analysis of the population time series of five butterfly species indicated that (meta)population dynamics are driven by density-dependent factors. Inter-specific comparison reveals a significant inverse relationship between population growth rate and the magnitude of dispersal distance. As the range of dispersal distances is constrained by the patch system, dispersing individuals moving too far away would (probably) get lost. This generates selective pressures on individuals with a high dispersal propensity, but favors individuals investing more in reproduction and results in a higher (meta)population growth rate. From a conservation perspective, individuals from (meta)populations and species sacrificing dispersal for the sake of reproductive performances are most vulnerable because of their higher sensitivity to stochastic events: the temporal variation of growth rate was much higher in the two metapopulations where dispersal was limited.

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.