Glanville Fritillary Butterfly Melitaea Cinxia Research Articles

Self-segregation in heterogeneous metapopulation landscapes

Complex interactions are at the root of the population dynamics of many natural systems, particularly for being responsible for the allocation of species and individuals across apposite niches of the ecological landscapes. On the other side, the randomness that unavoidably characterises complex systems has increasingly challenged the niche paradigm providing alternative neutral theoretical models. We introduce a network-inspired metapopulation individual-based model (IBM), hereby named self-segregation, where the density of individuals in the hosting patches (local habitats) drives the individuals spatial assembling while still constrained by nodes’ saturation. In particular, we prove that the core–periphery structure of the networked landscape triggers the spontaneous emergence of vacant habitat patches, which segregate the population in multistable patterns of isolated (sub)communities separated by empty patches. Furthermore, a quantisation effect in the number of vacant patches is observed once the total system mass varies continuously, emphasising thus a striking feature of the robustness of population stationary distributions. Notably, our model reproduces the patch vacancy found in the fragmented habitat of the Glanville fritillary butterfly Melitaea cinxia, an endemic species of the Åland islands. We argue that such spontaneous breaking of the natural habitat supports the concept of the highly contentious (Grinnellian) niche vacancy and also suggests a new mechanism for the endogeneous habitat fragmentation and consequently the peripatric speciation.

Microclimatic variability buffers butterfly populations against increased mortality caused by phenological asynchrony between larvae and their host plants

Climate change affects insects in several ways, including phenological shifts that may cause asynchrony between herbivore insects and their host plants. Insect larvae typically have limited movement capacity and are consequently dependent on the microhabitat conditions of their immediate surroundings. Based on intensive field monitoring over two springs and on larger‐scale metapopulation‐level survey over the same years, we used Bayesian spatial regression modelling to study the effects of weather and microclimatic field conditions on the development and survival of post‐diapause larvae of the Glanville fritillary butterflyMelitaea cinxiaon its northern range edge. Moreover, we assessed whether the observed variation in growth and survival in a spring characterized by exceptionally warm weather early in the season translated into population dynamic effects on the metapopulation scale. While similar weather conditions enhanced larval survival and growth rate in the spring, microclimatic conditions affected survival and growth contrastingly due to the phenological asynchrony between larvae and their host plants in microclimates that supported fastest growth. In the warmest microclimates, larvae reached temperatures over 20°C above ambient leading to increased feeding, which was not supported by the more slowly growing host plants. At the metapopulation level, population growth rate was highest in local populations with heterogeneous microhabitats. We demonstrate how exceptionally warm weather early in the spring caused a phenological asynchrony between butterfly larvae and their host plants. Choice of warmest microhabitats for oviposition is adaptive under predominant conditions, but it may become maladaptive if early spring temperatures rise. Such conditions may lead to larvae breaking diapause earlier without equally advancing host plant growth. Microclimatic variability within and among populations is likely to have a crucial buffering effect against climate change in many insects.

Host-plant availability drives the spatiotemporal dynamics of interacting metapopulations across a fragmented landscape.

The dynamics of ecological communities depend partly on species interactions within and among trophic levels. Experimental work has demonstrated the impact of species interactions on the species involved, but it remains unclear whether these effects can also be detected in long‐term time series across heterogeneous landscapes. We analyzed a 19‐yr time series of patch occupancy by the Glanville fritillary butterfly Melitaea cinxia, its specialist parasitoid wasp Cotesia melitaearum, and the specialist fungal pathogen Podosphaera plantaginis infecting Plantago lanceolata, a host plant of the Glanville fritillary. These species share a network of more than 4,000 habitat patches in the Åland islands, providing a metacommunity data set of unique spatial and temporal resolution. To assess the influence of interactions among the butterfly, parasitoid, and mildew on metacommunity dynamics, we modeled local colonization and extinction rates of each species while including or excluding the presence of potentially interacting species in the previous year as predictors. The metapopulation dynamics of all focal species varied both along a gradient in host plant abundance, and spatially as indicated by strong effects of local connectivity. Colonization and to a lesser extent extinction rates depended also on the presence of interacting species within patches. However, the directions of most effects differed from expectations based on previous experimental and modeling work, and the inferred influence of species interactions on observed metacommunity dynamics was limited. These results suggest that although local interactions among the butterfly, parasitoid, and mildew occur, their roles in metacommunity spatiotemporal dynamics are relatively weak. Instead, all species respond to variation in plant abundance, which may in turn fluctuate in response to variation in climate, land use, or other environmental factors.

Narrow oviposition preference of an insect herbivore risks survival under conditions of severe drought

Abstract Understanding species' habitat preferences are crucial to predict organisms' responses to the current climate crisis. In many insects, maternal habitat selection for oviposition essentially determines offspring performance. Whether future changes in climatic conditions may generate mismatches between oviposition preference and offspring performance, when mothers continue to prefer microhabitats that might threaten offspring survival, is an open question. To address this gap, we tested if oviposition preferences of the Glanville fritillary butterfly Melitaea cinxia females put offspring at risk when plants are under drought stress conditions. Mainly, we focus on identifying the microhabitat determinants for oviposition and the variation of conditions experienced by the sessile offspring, using field observations from 12 populations collected over 2015–2018. These data are combined with 10 years of larval nest and precipitation data to understand within‐population patterns of habitat selection. We tested whether the preferred microhabitats maximized the extended larval performance (i.e. overwinter survival). We found that females preferentially oviposited in microhabitats with higher host plant abundance and higher proportion of host plants with signs of drought stress. In most years, larval nests had higher survival in these drought‐stressed microhabitats. However, in an extremely dry year, only two nests survived over the summer. Our results highlight that a failure to shift habitat preference under extreme climate conditions may have drastic consequences for the survival of natural populations under changing climatic conditions. A free Plain Language Summary can be found within the Supporting Information of this article.

Long‐term demographic surveys reveal a consistent relationship between average occupancy and abundance within local populations of a butterfly metapopulation

Species distribution models are the tool of choice for large‐scale population monitoring, environmental association studies and predictions of range shifts under future environmental conditions. Available data and familiarity of the tools rather than the underlying population dynamics often dictate the choice of specific method – especially for the case of presence–absence data. Yet, for predictive purposes, the relationship between occupancy and abundance embodied in the models should reflect the actual population dynamics of the modelled species. To understand the relationship of occupancy and abundance in a heterogeneous landscape at the scale of local populations, we built a spatio‐temporal regression model of populations of the Glanville fritillary butterfly Melitaea cinxia in a Baltic Sea archipelago. Our data comprised nineteen years of habitat surveys and snapshot data of land use in the region. We used variance partitioning to quantify relative contributions of land use, habitat quality and metapopulation covariates. The model revealed a consistent and positive, but noisy relationship between average occupancy and mean abundance in local populations. Patterns of abundance were highly variable across years, with large uncorrelated random variation and strong local population stochasticity. In contrast, the spatio‐temporal random effect, habitat quality, population connectivity and patch size explained variation in occupancy, vindicating metapopulation theory as the basis for modelling occupancy patterns in fragmented landscapes. Previous abundance was an important predictor in the occupancy model, which points to a spillover of abundance into occupancy dynamics. While occupancy models can successfully model large‐scale population structure and average occupancy, extinction probability estimates for local populations derived from occupancy‐only models are overconfident, as extinction risk is dependent on actual, not average, abundance.

Life history alterations upon oral and hemocoelic bacterial exposure in the butterfly Melitaea cinxia.

Life history strategies often shape biological interactions by specifying the parameters for possible encounters, such as the timing, frequency, or way of exposure to parasites. Consequentially, alterations in life‐history strategies are closely intertwined with such interaction processes. Understanding the connection between life‐history alterations and host–parasite interactions can therefore be important to unveil potential links between adaptation to environmental change and changes in interaction processes. Here, we studied how two different host–parasite interaction processes, oral and hemocoelic exposure to bacteria, affect various life histories of the Glanville fritillary butterfly Melitaea cinxia. We either fed or injected adult butterflies with the bacterium Micrococcus luteus and observed for differences in immune defenses, reproductive life histories, and longevity, compared to control exposures. Our results indicate differences in how female butterflies adapt to the two exposure types. Orally infected females showed a reduction in clutch size and an earlier onset of reproduction, whereas a reduction in egg weight was observed for hemocoelically exposed females. Both exposure types also led to shorter intervals between clutches and a reduced life span. These results indicate a relationship between host–parasite interactions and changes in life‐history strategies. This relationship could cast restrictions on the ability to adapt to new environments and consequentially influence the population dynamics of a species in changing environmental conditions.

A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.

Variation in heat shock protein expression at the latitudinal range limits of a widely‐distributed species, the Glanville fritillary butterfly (Melitaea cinxia)

AbstractStudies of heat shock response show a correlation with local climate, although this is more often across altitudinal than latitudinal gradients. In the present study, differences in constitutive but not inducible components of heat shock response are detected among populations of the Glanville fritillary butterfly Melitaea cinxia L. that exist at the species' latitudinal range limits (Finland and Spain). The study demonstrates that macroclimatic differences between these sites should cause greater exposure of the Spanish population to higher temperatures. Thermal stress treatments are used to estimate differences in the expression of four genes potentially relevant for tolerating these temperatures. For the analysis, three heat‐shock proteins and glyceraldehyde‐3‐phosphate dehydrogenase (G3PDH), a glycolysis enzyme that also modulates cell growth based on metabolic state, are chosen. Two constitutive differences are found between the sites. First, insects from Spain have higher levels of Hsp 21.4 than those from Finland regardless of thermal stress treatment; this protein is not inducible. Second, insects from Finland have higher levels of G3PDH. The two remaining Hsps, Hsp20.4 and Hsp90, show dramatic up‐regulation at higher temperatures, although there are no significant differences between insects from the different populations in either constitutive levels or inducibility. In nature, differences between the study populations likely occur in the expression of all four genes that were studied, although these differences would be directly climate‐induced in Hsp20.4 and Hsp90 and constitutive in Hsp21.4 and G3PDH. Inducibility may mitigate the need for constitutive variation in traits that adapt insects to local climate.

Microsatellites for the parasitoid wasp Hyposoter horticola

We developed 14 microsatellite loci for the solitary parasitoid wasp Hyposoter horticola, an egg-larval endoparasitoid specialist of the Glanville fritillary butterfly Melitaea cinxia, in the Aland islands, Finland. The microsatellites were developed from a 454 sequencing enriched library. The characteristics of the primer sets and polymerase chain reactions for these microsatellite markers are presented. Thirteen of the 14 loci tested were polymorphic with on average 3.6 alleles per locus (range 3–6). The expected (HE) and observed (HO) heterozygosities ranged from 0.19 to 0.76 and 0.20 to 0.62 respectively. These markers can be used to study population genetics and genetic relatedness in H. horticola or related taxa, and to assess the presence of the parasitoid in hosts.

Direct and trans-generational responses to food deprivation during development in the Glanville fritillary butterfly

Life history characteristics and resulting fitness consequences manifest not only in an individual experiencing environmental conditions but also in its offspring via trans-generational effects. We conducted a set of experiments to assess the direct and trans-generational effects of food deprivation in the Glanville fritillary butterfly Melitaea cinxia. Food availability was manipulated during the final stages of larval development and performance was assessed during two generations. Direct responses to food deprivation were relatively minor. Food-deprived individuals compensated, via increased development time, to reach a similar mass as adults from the control group. Delayed costs of compensatory growth were observed, as food-deprived individuals had either reduced fecundity or lifespan depending on the type of feeding treatment they had experienced (intermittent vs. continuous). Female food deprivation did not directly affect her offspring's developmental trajectory, but the way the offspring coped with food deprivation. Offspring of mothers from control or intermittent starvation treatments reached the size of those in the control group via increased development time when being starved. In contrast, offspring of mothers that had experienced 2 days of continuous food deprivation grew even larger than control animals, when deprived of food themselves. Offspring of food-deprived Glanville fritillary initially showed poor immune response to parasitism, but not later on in development.

Size and genetic composition of the colonizing propagules in a butterfly metapopulation

The amount and spatial distribution of genetic variation that is maintained in a metapopulation depends critically on the colonization process. Here, we use molecular markers to determine the number and genetic relatedness of individuals establishing new local populations in a large metapopulation of the Glanville fritillary butterfly Melitaea cinxia. The empirical results are compared with the predictions of a dispersal model based on a diffusion approximation of correlated random walk, which serves as a base‐line hypothesis about the rate and pattern of colonization. The results show that half of the new local populations consisted of a single larval group of full sibs and hence necessarily of the offspring of a single female. If the colonization involved two or more larval groups, these were usually oviposited by two different females that were unrelated to each other. The pattern of colonizations is thus intermediate between the propagule pool and the migrant pool models. These results elucidate the generation of genetic stochasticity, which may influence the dynamics of small populations. The dispersal model predicted well the pattern of habitat occupancy and the pattern of colonizations in relation to landscape structure, though which particular habitat patches became colonized was influenced also by measures of habitat quality not included in the model.

Olfactory Attraction of the Larval Parasitoid,Hyposoter horticola, to Plants Infested with Eggs of the Host Butterfly,Melitaea cinxia

Parasitoids locate inconspicuous hosts in a heterogeneous habitat using plant volatiles, some of which are induced by the hosts. Hyposoter horticola Gravenhost (Hymenoptera: Ichneumonidae) is a parasitoid of the Glanville fritillary butterfly Melitaea cinxia L. (Lepidoptera: Nymphalidae). Melitaea cinxia lays eggs in clusters on leaves of Plantago lanceolata L. (Lamiales: Plantaginaceae) and Veronica spicata L. (Lamiales: Plantaginaceae). The parasitoid oviposits into host larvae that have not yet hatched from the egg. Thus, though H. horticola is a parasitoid of Melitaea cinxia larvae, it must find host eggs on plants that have not been fed on by the larvae. Using a Y-tube olfactometer, the response of H. horticola to odors of Melitaea cinxia and extracts of the attacked plant species were tested. Three week-old eggs (near hatching) were attractive to young H. horticola, but one week-old eggs were attractive only to old or experienced H. horticola. Melitaea cinxia larvae were not attractive. A water extract of P. lanceolata was attractive, but ethanol or hexane extracts were not. None of the extracts of V. spicata were attractive. Leaves of V. spicata were attractive only if harboring eggs, but P. lanceolata leaves with eggs were not. Free flying H. horticola in a large outdoor enclosure were presented with host and plant cues. As in the olfactometer, V. spicata was attractive only when eggs were on it, and P. lanceolata was somewhat attractive with or without eggs. This study shows for the first time that a parasitoid of larvae uses egg volatiles or oviposition-induced plant volatiles, to find host larvae, and that Melitaea cinxia eggs or traces of oviposition induce the production of these volatiles by the plant. Based on the results, and given the natural distribution of the plants and M. cinxia eggs, parasitism of Melitaea cinxia eggs on P. lanceolata would be expected to be low. Instead, under natural conditions, a fraction of the eggs in virtually all egg clusters are parasitized on both plant species. The mismatch between the experimental results and the natural pattern of host-parasitoid interactions is discussed in terms of the expected coupling foraging cues with foraging success.

The association between wing morphology and dispersal is sex-specific in the glanville fritillary butterfly Melitaea cinxia (Lepidoptera: Nymphalidae)

We examined whether dispersal was associated with body and wing morphology and individual quality, and whether such an association was sex-specific, in the Glanville fritillary butterfly Melitaea cinxia (L.) in Paldiski on the north coast of Estonia. Body weight, size and shape of both fore- and hindwing, wing aspect ratio and wing loading were used as measures of body and wing morphology. Fluctuating asymmetry (FA) of wing shape was used as a measure of individual quality. Males and females did not differ in dispersal rates, despite large differences in overall morphology and FA. Females had a significantly higher wing loading and aspect ratio, but a lower FA than males. Females, but not males, that dispersed differed in forewing shape from those that did not disperse. The sex-specifity of the covariation between dispersal and forewing shape is most probably due to wing shape being associated with different life-history traits in both sexes, resulting in different selection pressures on wing shape in each of the sexes.

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.

Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore.

The Glanville fritillary butterfly Melitaea cinxia feeds upon two host plant species in Aland, Finland, Plantago lanceolata and Veronica spicata, both of which produce iridoid glycosides. Iridoids are known to deter feeding or decrease the growth rate of many generalist insect herbivores, but they often act as oviposition cues to specialist butterflies and are feeding stimulants to their larvae. In this study, two iridoid glycosides (aucubin and catalpol) were analyzed by micellar electrokinetic capillary chromatography. We measured the spatial and temporal variation of iridoid glycosides in natural populations of the host plants of M. cinxia. We also analyzed the aucubin and catalpol content in plants in relation to their use by ovipositing females, and in relation to the incidence of parasitism of M. cinxia larvae in natural populations. The mean concentrations of aucubin and catalpol were higher in P. lanceolata than in V. spicata, and catalpol concentrations were higher than aucubin concentrations in both host species. Plantago lanceolata individuals that were used for oviposition by M. cinxia had higher aucubin concentrations than random plants and neighboring plants. Additionally, oviposition and random plants had higher catalpol concentrations than neighboring plants, indicating that ovipositing females select for high iridoid glycoside plants or that oviposition induces iridoid glycoside production in P. lanceolata. Parasitism by the specialist parasitoid wasp Cotesia melitaearum occurred most frequently in larval groups that were feeding on plants with low concentrations of catalpol, irrespective of year, population, and host plant species. Therefore, parasitoids appear to avoid or perform poorly in host larvae with high catalpol content.