Area-dependent migration by ringlet butterflies generates a mixture of patchy population and metapopulation attributes

Interpretation of spatially structured population systems is critically dependent on levels of migration between habitat patches. If there is considerable movement, with each individual visiting several patches, there is one ”patchy population”; if there is intermediate movement, with most individuals staying within their natal patch, there is a metapopulation; and if (virtually) no movement occurs, then the populations are separate (Harrison 1991, 1994). These population types actually represent points along a continuum of much to no mobility in relation to patch structure. Therefore, interpretation of the effects of spatial structure on the dynamics of a population system must be accompanied by information on mobility. We use empirical data on movements by ringlet butterflies, Aphantopus hyperantus, to investigate two key issues that need to be resolved in spatially-structured population systems. First, do local habitat patches contain largely independent local populations (the unit of a metapopulation), or merely aggregations of adult butterflies (as in patchy populations)? Second, what are the effects of patch area on migration in and out of the patches, since patch area varies considerably within most real population systems, and because human landscape modification usually results in changes in habitat patch sizes? Mark-release-recapture (MRR) data from two spatially structured study systems showed that 63% and 79% of recaptures remained in the same patch, and thus it seems reasonable to call both systems metapopulations, with some capacity for separate local dynamics to take place in different local patches. Per capita immigration and emigration rates declined with increasing patch area, while the resident fraction increased. Actual numbers of emigrants either stayed the same or increased with area. The effect of patch area on movement of individuals in the system are exactly what we would have expected if A. hyperantus were responding to habitat geometry. Large patches acted as local populations (metapopulation units) and small patches simply as locations with aggregations (units of patchy populations), all within 0.5 km². Perhaps not unusually, our study system appears to contain a mixture of metapopulation and patchy-population attributes.     

Finite metapopulation models with density-dependent migration and stochastic local dynamics

The effects of small density-dependent migration on the dynamics of a metapopulation are studied in a model with stochastic local dynamics. We use a diffusion approximation to study how changes in the migration rate and habitat occupancy affect the rates of local colonization and extinction. If the emigration rate increases or if the immigration rate decreases with local population size, a positive expected rate of change in habitat occupancy is found for a greater range of habitat occupancies than when the migration is density-independent. In contrast, the reverse patterns of density dependence in respective emigration and immigration reduce the range of habitat occupancies where the metapopulation will be viable. This occurs because density-dependent migration strongly influences both the establishment and rescue effects in the local dynamics of metapopulations.     

Spatial scale of local adaptation in a plant-pathogen metapopulation

The rate and scale of gene flow can strongly affect patterns of local adaptation in host-parasite interactions. I used data on regional pathogen occurrence to infer the scale of pathogen dispersal and to identify pathogen metapopulations in the interaction between Plantago lanceolata and its specialist phytopathogen, Podosphaera plantaginis. Frequent extinctions and colonizations were recorded in the metapopulations, suggesting substantial gene flow at this spatial scale. The level of pathogen local adaptation was assessed in a laboratory inoculation experiment at three different scales: in sympatric host populations, in sympatric host metapopulations and in allopatric host metapopulations. I found evidence for adaptation to sympatric host populations, as well as evidence indicating that local adaptation may extend to the scale of the sympatric host metapopulation. There was also variation among the metapopulations in the degree of pathogen local adaptation. This may be explained by regional differences in the rate of migration.     

Potential metapopulation structure and the effects of habitat quality on population size of the endangered False Ringlet butterfly

The False Ringlet (Coenonympha oedippus) is a European butterfly species, endangered due to the severe loss and fragmentation of its habitat. In Hungary, two remaining populations of the butterfly occur in lowland Purple Moorgrass meadows. We studied a metapopulation occupying twelve habitat patches in Central Hungary. Our aim was to reveal what measures of habitat quality affect population size and density of this metapopulation, estimate dispersal parameters and describe phenology of subpopulations. Local population sizes and dispersal parameters were estimated from an extensive mark–release–recapture dataset, while habitat quality was characterized by groundwater level, cover of grass tussocks, bush cover, height of vegetation and grass litter at each habitat patch. The estimated size of the metapopulation was more than 3,000 individuals. We estimated a low dispersal capacity, especially for females, indicating a very low probability of (re)colonization. Butterfly abundance and density in local populations increased with higher grass litter, lower groundwater level and larger area covered by tussocks. We suppose that these environmental factors affect butterfly abundance by determining the microclimatic conditions for both larvae and adult butterflies. Our results suggest that the long-term preservation of the studied metapopulation needs the maintenance of high quality habitat patches by appropriate mowing regime and water regulation. Management also should facilitate dispersal to strengthen metapopulation structure with creating stepping-stones or gradually increase habitat quality in present matrix.     

Parasites promote host gene flow in a metapopulation

Local adaptation is a powerful mechanism to maintain genetic diversity in subdivided populations. It counteracts the homogenizing effect of gene flow because immigrants have an inferior fitness in the new habitat. This picture may be reversed in host populations where parasites influence the success of immigrating hosts. Here we report two experiments testing whether parasite abundance and genetic background influences the success of host migration among pools in a Daphnia magna metapopulation. In 22 natural populations of D. magna, immigrant hosts were found to be on average more successful when the resident populations experienced high prevalences of a local microsporidian parasite. We then determined whether this success is due to parasitism per se, or the genetic background of the parasites. In a common garden competition experiment, we found that parasites reduced the fitness of their local hosts relatively more than the fitness of allopatric host genotypes. Our experiments are consistent with theoretical predictions based on coevolutionary host-parasite models in metapopulations. A direct consequence of the observed mechanism is an elevated effective migration rate for the host in the metapopulation.     

Higher mobility of butterflies than moths connected to habitat suitability and body size in a release experiment

Mobility is a key factor determining lepidopteran species responses to environmental change. However, direct multispecies comparisons of mobility are rare and empirical comparisons between butterflies and moths have not been previously conducted. Here, we compared mobility between butterflies and diurnal moths and studied species traits affecting butterfly mobility. We experimentally marked and released 2011 butterfly and 2367 moth individuals belonging to 32 and 28 species, respectively, in a 25 m × 25 m release area within an 11‐ha, 8‐year‐old set‐aside field. Distance moved and emigration rate from the release habitat were recorded by species. The release experiment produced directly comparable mobility data in 18 butterfly and 9 moth species with almost 500 individuals recaptured. Butterflies were found more mobile than geometroid moths in terms of both distance moved (mean 315 m vs. 63 m, respectively) and emigration rate (mean 54% vs. 17%, respectively). Release habitat suitability had a strong effect on emigration rate and distance moved, because butterflies tended to leave the set‐aside, if it was not suitable for breeding. In addition, emigration rate and distance moved increased significantly with increasing body size. When phylogenetic relatedness among species was included in the analyses, the significant effect of body size disappeared, but habitat suitability remained significant for distance moved. The higher mobility of butterflies than geometroid moths can largely be explained by morphological differences, as butterflies are more robust fliers. The important role of release habitat suitability in butterfly mobility was expected, but seems not to have been empirically documented before. The observed positive correlation between butterfly size and mobility is in agreement with our previous findings on butterfly colonization speed in a long‐term set‐aside experiment and recent meta‐analyses on butterfly mobility.     

Non-random dispersal in the butterfly Maniola jurtina: implications for metapopulation models

The dispersal patterns of animals are important in metapopulation ecology because they affect the dynamics and survival of populations. Theoretical models assume random dispersal but little is known in practice about the dispersal behaviour of individual animals or the strategy by which dispersers locate distant habitat patches. In the present study, we released individual meadow brown butterflies (Maniola jurtina) in a non-habitat and investigated their ability to return to a suitable habitat. The results provided three reasons for supposing that meadow brown butterflies do not seek habitat by means of random flight. First, when released within the range of their normal dispersal distances, the butterflies orientated towards suitable habitat at a higher rate than expected at random. Second, when released at larger distances from their habitat, they used a non-random, systematic, search strategy in which they flew in loops around the release point and returned periodically to it. Third, butterflies returned to a familiar habitat patch rather than a non-familiar one when given a choice. If dispersers actively orientate towards or search systematically for distant habitat, this may be problematic for existing metapopulation models, including models of the evolution of dispersal rates in metapopulations.     

Three ways of assessing metapopulation structure in the butterfly Plebejus argus

1. Three independent methods were used to investigate population structure in the butterfly Plebejus argus . First, migration and dispersal ability were measured by mark–release–recapture in seven adjacent habitat patches, and by release of butterflies in unoccupied habitat. Secondly, colonization of newly created habitat was observed over 7 years. Finally, genetic differentiation of local populations within a metapopulation was investigated. Sampled local populations included parts of the mark–release–recapture study area.
2. Plebejus argus is relatively sedentary: the maximum movement detected was 395 m, and only 2% of individuals moved further than 100 m between recaptures on different days. None the less, adjacent local populations in the mark–release–recapture study area were linked by occasional migration, with ≈ 1.4% of individuals moving between patches separated by 13–200 m.
3. Despite low mobility, observed colonizations occurred rapidly over distances of 1 km. Because P. argus occurs at high population densities, 1.4% migration can generate enough migrants to colonize newly suitable habitat quickly at this spatial scale.
4. Mark–release–recapture data were used to predict that there would be limited genetic differentiation through drift between local populations at this spatial scale. The prediction was supported by allele frequency data for the same local populations.
5. Genetic differentiation often indicates higher levels of migration than are revealed by the movements of marked individuals. This study shows that when experimental releases and extensive marking are undertaken in areas that are large relative to most movements, indirect measures of gene flow and direct measures of dispersal can concur.
6. Evidence from the three different approaches was complementary, indicating that P. argus occurs as metapopulations within the study area.     

Functional genomics of life history variation in a butterfly metapopulation

In fragmented landscapes, small populations frequently go extinct and new ones are established with poorly understood consequences for genetic diversity and evolution of life history traits. Here, we apply functional genomic tools to an ecological model system, the well-studied metapopulation of the Glanville fritillary butterfly. We investigate how dispersal and colonization select upon existing genetic variation affecting life history traits by comparing common-garden reared 2-day adult females from new populations with those from established older populations. New-population females had higher expression of abdomen genes involved in egg provisioning and thorax genes involved in the maintenance of flight muscle proteins. Physiological studies confirmed that new-population butterflies have accelerated egg maturation, apparently regulated by higher juvenile hormone titer and angiotensin converting enzyme mRNA, as well as enhanced flight metabolism. Gene expression varied between allelic forms of two metabolic genes (Pgi and Sdhd), which themselves were associated with differences in flight metabolic rate, population age and population growth rate. These results identify likely molecular mechanisms underpinning life history variation that is maintained by extinction-colonization dynamics in metapopulations.     

Evidence for positive density-dependent emigration in butterfly metapopulations

A positive effect of (meta)population density on emigration has been predicted by many theoretical models and confirmed empirically in various organisms. However, in butterflies, the most popular species for dispersal studies, the evidence for its existence has so far been equivocal, with negative relationships between density and emigration being reported more frequently. We analysed dispersal in sympatric metapopulations of two Maculinea butterflies, intensively surveyed with mark–release–recapture methods for 7 years. Dispersal parameters, derived using the virtual migration model, were assessed against butterfly densities, which fluctuated strongly over the study period. Emigration was positively correlated with density, and this effect was particularly strong at densities above carrying capacity, when emigration increased up to threefold in females and twofold in males compared with the normal levels. In turn, density had little impact on other dispersal parameters analysed. Our findings provide good evidence for positive density-dependence of emigration in butterflies. Emigrating at high densities is particularly beneficial for females, because it gives them a chance to lay part of their egg-load in less crowded patches, where offspring survival is higher due to lower intraspecific competition. Even though the rise in emigration becomes considerable at densities exceeding carrying capacity, i.e. relatively infrequently, it still has serious implications for many ecological phenomena, such as species range expansions, gene flow, and metapopulation persistence. Consequently, instead of treating emigration as a fixed trait, it is worth allowing for its density-dependence in applications such as population viability analyses, genetic models or metapopulation models.     

Dispersal-related life-history trade-offs in a butterfly metapopulation

1. Recent studies on butterflies have documented apparent evolutionary changes in dispersal rate in response to climate change and habitat change. These studies often assume a trade-off between dispersal rate (or flight capacity) and reproduction, which is the rule in wing-dimorphic species but might not occur equally in wing-monomorphic species such as butterflies. 2. To investigate the relationship between dispersal rate and fecundity in the Glanville fritillary butterfly Melitaea cinxia we recorded lifetime individual movements, matings, ovipositions, and maximal life span in a large (32 x 26 m) population cage in the field. Experimental material was obtained from 20 newly established and 20 old local populations within a large metapopulation in the Aland Islands in Finland. 3. Females of the Glanville fritillary from newly established populations are known to be more dispersive in the field, and in the cage they showed significantly greater mobility, mated earlier, and laid more egg clutches than females from old populations. The dispersive females from new populations exhibited no reduced lifetime fecundity in the cage, but they had a shorter maximal life span than old-population females. 4. These results challenge the dispersal-fecundity trade-off for nonmigratory butterflies but instead suggest a physiological trade-off between high metabolic performance and reduced maximal life span. High metabolic performance may explain high rates of dispersal and oviposition in early life. 5. In fragmented landscapes, an ecological trade-off exists between being more dispersive and hence spending more time in the landscape matrix vs. having more time for reproduction in the habitat. We estimate with a dispersal model parameterized for the Glanville fritillary that the lifetime egg production is 4% smaller on average in the more dispersive butterflies in a representative landscape, with much variation depending on landscape structure in the neighbourhood of the natal patch, from--26 to 45% in the landscape analysed in this paper.     

What is a patch in a dynamic metapopulation? Mobility of an endangered woodland butterfly,Euphydryas maturna

In metapopulations of butterflies inhabiting transient forest openings, the dynamic character of biotopes prevents unequivocal delimitation of habitat patches, complicating analyses of inter-patch dispersal. We analyse mobility of one such metapopulation, using mark-recapture data on an endangered butterfly, the scarce fritillary Euphydryas maturna , at its last site in the Czech Republic. The butterfly inhabits woodland clearings, its population numbered 190 individuals in 2002. We modelled movements in eight habitat patchworks delimited according to different criteria and superimposed over the forest, using the Virtual Migration model. Resulting mobility parameters were generally robust against patchwork definitions, the main distinction was between patchworks based on presence of adults and consisting of small patches and patchworks based on distributions of larval nests and consisting of large patches. Emigration constant decreased towards the latter, whereas males suffered higher migration mortality than females in the former. Patchworks delimited according to presence of adults performed better than patchworks based on distribution of larval nests. A comparison of our parameters with those found for the species in Finland showed that the Czech butterflies were more prone to leave individual patches and suffered higher migration mortality, which combined into considerably shorter survival. We conclude that transferring dispersal parameters among different regions and populations is more risky than using less suitable definitions of habitat patches within single region.     

Migration of moth species in a network of small islands

Rapidly increasing fragmentation of natural landscapes decreases the ability of many species to reach the smaller and more isolated patches of habitat in a metapopulation. The densities of local populations of several moth species and the butterfly Hipparchia semele in a network of small islands, and the rates of inter-island movement and movement patterns, were investigated, to determine the factors affecting the rate and pattern of movements. The estimated population densities ranged from 0.001 to 0.2 individuals/m². The observed emigration and immigration rates depended on island isolation and various traits of the species, with great variability in migration rates among species. Thin-bodied, slow-flying species did not move among the islands, whereas many robust, fast-flying species moved among the islands relatively frequently. Migration rate increased significantly with body size and was significantly higher in oligophagous than in polyphagous species, suggesting that these factors are important determinants of the migration rate of the species. Migration rate was low when the surface temperature of the sea was low, and a greater proportion of individuals emigrated from small than large patches of habitat. The migration distances of female noctuids were shorter than those of males and those of both sexes of the butterfly H. semele. The observed movement patterns are consistent with a metapopulation structure in most of the moth species.     

Population structure of a large blue butterfly and its specialist parasitoid in a fragmented landscape

Habitat fragmentation may interrupt trophic interactions if herbivores and their specific parasitoids respond differently to decreasing connectivity of populations. Theoretical models predict that species at higher trophic levels are more negatively affected by isolation than lower trophic level species. By combining ecological data with genetic information from microsatellite markers we tested this hypothesis on the butterfly Maculinea nausithous and its specialist hymenopteran parasitoid Neotypus melanocephalus. We assessed the susceptibility of both species to habitat fragmentation by measuring population density, rate of parasitism, overall genetic differentiation (theta(ST)) and allelic richness in a large metapopulation. We also simulated the dynamics of genetic differentiation among local populations to asses the relative effects of migration rate, population size, and haplodiploid (parasitoid) and diploid (host) inheritance on metapopulation persistence. We show that parasitism by N. melanocephalus is less frequent at larger distances to the nearest neighbouring population of M. nausithous hosts, but that host density itself is not affected by isolation. Allelic richness was independent of isolation, but the mean genetic differentiation among local parasitoid populations increased with the distance between these populations. Overall, genetic differentiation in the parasitoid wasp was much greater than in the butterfly host and our simulations indicate that this difference is due to a combination of haplodiploidy and small local population sizes. Our results thus support the hypothesis that Neotypus parasitoid wasps are more sensitive to habitat fragmentation than their Maculinea butterfly hosts.     

Life history of the Glanville fritillary butterfly in fragmented versus continuous landscapes

Habitat loss and fragmentation threaten the long‐term viability of innumerable species of plants and animals. At the same time, habitat fragmentation may impose strong natural selection and lead to evolution of life histories with possible consequences for demographic dynamics. The Baltic populations of the Glanville fritillary butterfly (Melitaea cinxia) inhabit regions with highly fragmented habitat (networks of small dry meadows) as well as regions with extensive continuous habitat (calcareous alvar grasslands). Here, we report the results of common garden studies on butterflies originating from two highly fragmented landscapes (FL) in Finland and Sweden and from two continuous landscapes (CL) in Sweden and Estonia, conducted in a large outdoor cage (32 by 26 m) and in the laboratory. We investigated a comprehensive set of 51 life‐history traits, including measures of larval growth and development, flight performance, and adult reproductive behavior. Seventeen of the 51 traits showed a significant difference between fragmented versus CL. Most notably, the growth rate of postdiapause larvae and several measures of flight capacity, including flight metabolic rate, were higher in butterflies from fragmented than CL. Females from CL had shorter intervals between consecutive egg clutches and somewhat higher life‐time egg production, but shorter longevity, than females from FL. These results are likely to reflect the constant opportunities for oviposition in females living in continuous habitats, while the more dispersive females from FL allocate more resources to dispersal capacity at the cost of egg maturation rate. This study supports theoretical predictions about small population sizes and high rate of population turnover in fragmented habitats selecting for increased rate of dispersal, but the results also indicate that many other life‐history traits apart from dispersal are affected by the degree of habitat fragmentation.     

Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) are widely distributed and a high degree of morphometric and genetic differentiation has been found among both allopatric and parapatric populations. We analysed 145 samples along a contiguous distributional range from the Black Sea to the eastern North Atlantic for mitochondrial and nuclear genetic diversity, and found population structure with boundaries that coincided with transitions between habitat regions. These regions can be characterized by ocean floor topography, and oceanographic features such as surface salinity, productivity and temperature. At the extremes of this range there was evidence for the directional emigration of females. Bi-parentally inherited markers did not show this directional bias in migration, suggesting a different dispersal strategy for males and females at range margins. However, comparative assessment based on mitochondrial DNA and nuclear markers indicated that neither sex showed a strong bias for greater dispersal on average. These data imply a mechanism for the evolutionary structuring of populations based on local habitat dependence for both males and females.     

Contrasting movement patterns in two species of chequerspot butterflies, Euphydryas aurinia and Melitaea phoebe, in the same patch network

Abstract.  1. Mark–release–recapture studies were conducted on two species of chequerspot butterfly, Euphydryas aurinia and Melitaea phoebe , in the same habitat patch network in Yanjiaping, a small basin in the Taihang Mountains, north-west of Beijing, China, in 2000.
2. Euphydryas aurinia tended to stay in the habitat patches and to move to neighbouring patches, whereas M. phoebe moved widely among patches in the entire network.
3. The parameters of the virtual migration model showed higher daily emigration propensity in M. phoebe and in E. aurinia males than in E. aurinia females, and significantly greater average daily movement distance in M. phoebe than in E. aurinia .
4. The results are consistent with the previous findings showing genetic structuring among local populations of E. aurinia but not among local populations of M. phoebe .
5. Based on the genetic and ecological results, it was concluded that E. aurinia has a classic metapopulation in the study area, whereas M. phoebe appears to have a source–sink metapopulation.
6. In 2000, when there was an overall increase in the abundance of the two species, the limited mobility of E. aurinia resulted in an increase in the average local population size, whereas the increase in the number of local populations in M. phoebe was due to its high mobility .     

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.     

Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites. Traditionally parasite local adaptation has been investigated in field transplant experiments or in the laboratory under a constant environment. Despite the conceptual importance of local adaptation in studies of (co)evolution, to date no study has provided a comparative analysis of these two methods. Here, using information on pathogen population dynamics, I tested local adaptation of the specialist phytopathogen, Podosphaera plantaginis, to its host, Plantago lanceolata at three different spatial scales: sympatric host population, sympatric host metapopulation and allopatric host metapopulations. The experiment was carried out as a field transplant experiment with greenhouse-reared host plants from these three different origins introduced into four pathogen populations. In contrast to results of an earlier study performed with these same host and parasite populations under laboratory conditions, I did not find any evidence for parasite local adaptation. For interactions governed by strain-specific resistance, field studies may not be sensitive enough to detect mean parasite population virulence. Given that parasite transmission potential may be mediated by the abiotic environment and genotype-by-environment interactions, I suggest that relevant environmental variation should be incorporated into laboratory studies of parasite local adaptation.     

Metapopulation structure and habitat quality in modelling dispersal in the butterfly Iolana iolas

Quantifying dispersal is fundamental to understanding the effects of fragmentation on populations. Although it has been shown that patch and matrix quality can affect dispersal patterns, standard metapopulation models are usually based on the two basic variables, patch area and connectivity. In 2004 we studied migration patterns among 18 habitat patches in central Spain for the butterfly Iolana iolas, using mark–release–recapture methods. We applied the virtual migration (VM) model and estimated the parameters of emigration, immigration and mortality separately for males and females. During parameter estimation and model simulations, we used original and modified patch areas accounting for habitat quality with three different indices. Two indices were based on adult and larval resources (flowers and fruits) and the other one on butterfly density. Based on unmodified areas, our results showed that both sexes were markedly different in their movements and mortality rates. Females emigrated more frequently from patches, but males that emigrated were estimated to move longer daily dispersal distances and suffer higher mortality than females during migration. Males were more likely to emigrate from small than from large patches, but patch area had no significant effect on female emigration. The effects of area on immigration rate and the within-patch mortality were similar in both sexes. Based on modified areas, the estimated parameter values and the model simulation results were similar to those estimated using the unmodified patch areas. One possible reason for the failure to significantly improve the parameter estimates of the VM model is the fact that resource quantity and butterfly population sizes were strongly correlated with patch area. Our results suggest that the standard VM modelling approach, based on patch area and connectivity, can provide a realistic picture of the movement patterns of I. iolas .