Extinction-colonization dynamics and host-plant choice in butterfly metapopulations

Species living in highly fragmented landscapes often occur as metapopulations with frequent population turnover. Turnover rate is known to depend on ecological factors, such as population size and connectivity, but it may also be influenced by the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly (Melitaea cinxia) in Finland uses two host-plant species that vary in their relative abundances among distinct habitat patches (dry meadows) in a large network of approximately 1,700 patches. We found no effect of host species use on local extinction. In contrast, population establishment was strongly influenced by the match between the host species composition of an empty habitat patch and the relative host use by larvae in previous years in the habitat patches that were well connected to the target patch. This "colonization effect" could be due to spatially variable plant acceptability or resistance or to spatially variable insect oviposition preference or larval performance. We show that spatial variation in adult oviposition preference occurs at the relevant spatial scale and that the other possible causes of the colonization effect can be discounted. We conclude that the colonization effect is generated by host preference influencing the movement patterns of ovipositing females. Migrant females with dissimilar host preferences have different perceptions of relative patch quality, which influences their likelihood of colonizing patches with particular host composition.     

Patch dynamics ofGlaucopsyche lygdamus (Lycaenidae): correlations between butterfly density and host species diversity

Glaucopsyche lygdamus egg densities were surveyed over a 2000-m section of Gold Creek and at 30 different isolated patches in the Gold Basin drainage in Colorado. Host plant numbers and diversity were quantified, as well as other variables potentially influencing butterfly population size, such as patch size and isolation. Egg densities correlated significantly only with measures of host species diversity. Patches consisting of a single host species, no matter how large, did not support high butterfly densities, but patches of multiple, equitably distributed host species did. The most likely explantation, in light of oviposition preference and larval performance data accumulated for this butterfly species, is that host species diversity is necessary for the persistence ofG. lygdamus populations, because alternative host species buffer population losses during poor or unusual years. The dependence of both ovipositing butterflies and developing larvae on the ephemeral, young, host plant flowers make the butterfly especially vulnerable to year-to-year variation in host plant availability and quality.     

Consequences of exotic host use: impacts on Lepidoptera and a test of the ecological trap hypothesis

Investigating the effects of invasive species on native biodiversity is one of the most pressing challenges in ecology. Our goal in this study was to quantify the effects of invasive plants on butterfly and moth communities. In addition, we sought to elucidate the fitness consequences of non-native hosts on lepidopterans. We conducted a meta-analysis on a total of 76 studies which provided data on larval performance, survival, oviposition preference, abundance, and species richness of Lepidoptera on native and exotic plants. Overwhelmingly, we found that performance and survival were reduced for larvae developing on exotic hosts, relative to native hosts. At the community level, alien plant invasion was associated with a reduction in the overall abundance and richness of lepidopteran communities. We found that lepidopterans did not show strong oviposition preference for native hosts. This result suggests that many invasive plant species may decrease lepidopteran abundance by providing a target for oviposition where larvae have a relatively poor chance of survival. Among studies that tested both survival and preference on exotic hosts, 37.5 % found evidence for novel hosts that could function as ecological traps (the figure was 18 % when considering studies that only assayed larval performance). Thus, although the majority of novel hosts included in our analyses are not likely to act as ecological traps, the potential clearly exists for this effect, and the role of ecological traps should be considered along with other aspects of global change impacting natural communities.     

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.     

Restoration of an endangered plant,Hygrophila pogonocalyx,leads to an adaptive host shift of the chocolate pansy (Junonia iphita iphita)

Anthropogenic introduction of a plant species may cause novel encounters between the plant and local herbivores, and initiate evolutionary changes in host plant usage by herbivores. Until recently the endemic aquatic plant Hygrophila pogonocalyx was endangered and had a restricted distribution in Taiwan. Massive restoration efforts since 1997 have led to an expansion of the plant's distribution and a novel encounter between it and an Asian butterfly, the chocolate pansy, Junonia iphita (Nymphalidae). This butterfly appears to have colonized H. pogonocalyx, switching from its original host, Strobilanthes penstemonoides var. formosana. In the present study, we aimed to investigate whether the utilization of H. pogonocalyx as a host plant has initiated a differentiation between butterflies using the novel and the original hosts. To this purpose we collected butterflies from patches of the two host plants which grow sympatrically. We tested oviposition preference for the two hosts and larval performance on them. Female adults exhibited distinct oviposition preference toward the host plant their mothers preferred. Offspring showed greater survivorship and pupal weight when fed on the host plant their mothers preferred. Male adults displayed territorial behaviors on the host plant that their mothers had preferred. Finally, the survival rate of offspring produced from cross-mating between individuals with different host plant preference was lower than that of non-hybrids. Taken together, we suggest that genetic differentiation has occurred between individuals preferring H. pogonocalyx versus S. penstemonoides as host plants via host shifting. This process was likely induced by the mass restoration of the formerly rare and endangered plant species.     

Diversity–invasibility relationships across multiple scales in disturbed forest understoreys

Non-native plant species richness may be either negatively or positively correlated with native species due to differences in resource availability, propagule pressure or the scale of vegetation sampling. We investigated the relationships between these factors and both native and non-native plant species at 12 mainland and island forested sites in southeastern Ontario, Canada. In general, the presence of non-native species was limited: <20% of all species at a site were non-native and non-native species cover was <4% m⁻² at 11 of the 12 sites. Non-native species were always positively correlated with native species, regardless of spatial scale and whether islands were sampled. Additionally, islands had a greater abundance of non-native species. Non-native species richness across mainland sites was significantly negatively correlated with mean shape index, a measure of the ratio of forest edge to area, and positively correlated with the mean distance to the nearest forest patch. Other factors associated with disturbance and propagule pressure in northeastern North America forests, including human land use, white-tailed deer populations, understorey light, and soil nitrogen, did not explain non-native richness nor cover better than the null models. Our results suggest that management strategies for controlling non-native plant invasions should aim to reduce the propagule pressure associated with human activities, and maximize the connectivity of forest habitats to benefit more poorly dispersed native species.     

Heterogeneity of plant phenotypes caused by herbivore-specific induced responses influences the spatial distribution of herbivores

Abstract.  1. Herbivory can induce resistance in a plant and the induced phenotype may be disfavoured by subsequent herbivores. Yet, as the distance between plants in a population increases, limited mobility may make a herbivore more likely to feed and oviposit on host plants in its immediate surroundings.
2. The present study tested whether a herbivore's preference and distribution across plants with different induced phenotypes was influenced by the spatial distribution of plants. A fragmented population of Solanum dulcamara plants was created. This consisted of discrete, spatially separated patches with different histories of damage, either herbivory from adult flea beetles ( Psylliodes affinis ), tortoise beetles ( Plagiometriona clavata ), or mechanical damage. Each patch was separated by 7 m and consisted of 12 plants that were spaced 30 cm apart. Then a fixed number of adult tortoise beetles were introduced to each patch, and movement and oviposition within and between spatially separate homogeneous patches (receiving one type of damage) were compared with movement and oviposition within heterogeneous patches (containing all three types of damage) over the growing season.
3. Flea beetle and tortoise beetle herbivory consistently induced different phytochemical responses in S. dulcamara (polyphenol oxidase and peroxidase), and adult tortoise beetles avoided oviposition on the flea beetle induced plants within heterogeneous patches. However, between homogeneous patches, plant phenotype did not influence oviposition. Colonisation by naturally occurring flea beetle adults followed a similar pattern.
4. These results suggest that the heterogeneity of plant phenotypes can influence herbivore choice and distribution at small but not large spatial scales.     

Food plant density,patch isolation and vegetation height determine occurrence in a Swedish metapopulation of the marsh fritillary <Emphasis Type="Italic">Euphydryas aurinia</Emphasis> (Rottemburg, 1775) (Lepidoptera,Nymphalidae)

The occurrence pattern of the marsh fritillary was studied within a patch network on the Baltic island Öland, Sweden. Presence/absence was established for potentially suitable habitat patches (n = 158) on calcareous moist grassland and analyzed in a multiple logistic regression model where patch area, patch isolation and nine habitat quality variables were included as explanatory variables. Larval food plant density was positively, and patch isolation negatively, correlated to the presence of Euphydryas aurinia. Area did not contribute to the explanation of the occurrence pattern. Significant interactions between larval food plant density times patch isolation, and larval food plant density times vegetation height, show that with low food plant density the butterfly primarily occurs in patches with a vegetation height of 4–10 cm, within a distance of 250 m from nearest occupied patch. In patches with a high food plant density the butterfly occurs in patches where the vegetation height is higher, 4–16 cm, and the distance to nearest occupied patch can be longer, up to 1.4 km. This study supports earlier findings in other regions, suggesting that a network of adjacent patches with a high food plant density and a vegetation height within the preferred threshold, despite their size, is an apparent conservation goal.     

Host plant use by the Heath fritillary butterfly, Melitaea athalia: plant habitat, species and chemistry

We present a study of habitat use, oviposition plant choice, and food plant suitability for the checkerspot butterfly Melitaea athalia Rottemburg (Lepidoptera: Nymphalidae) in Åland, Finland. We found that in Åland, unlike in the mainland of Finland and many parts of its range, M. athalia flies mainly in open meadows. When offered an array of plants in a large (32 × 26 m) field cage, they predominately oviposited upon Veronica chamaedrys L., V. spicata L. and Plantago lanceolata L. (Plantaginaceae), which grow in open meadows. The relative abundance of the butterfly in Åland, and its habitat and host plant use there, may reflect local adaptation to land use practices and geology that maintain clusters of small open meadows with little successional change. At the scale of a plant patch, preferred species were used as frequently in mixed species patches as in mono-specific patches, and more oviposition occurred in open than in grassy patches. All of the host plants used by M. athalia are defended by iridoid glycosides (IGs). However, oviposition choice among species and among individual plants within species was largely independent of IG concentration. This contrast with the more discerning congener, M. cinxia, supports the idea that host discrimination decreases with increasing host range. Finally, although the adult butterflies chose specific plant species for oviposition, as larvae they performed well on twelve out of thirteen species of plants, including both known hosts and related novel plants that occur in Åland, indicating a much wider range of larval food plant species than adult oviposition species.     

Thyme and isolation for the Sinai baton blue butterfly (<Emphasis Type="Italic">Pseudophilotes sinaicus</Emphasis>)

The distribution of the narrowly endemic butterfly Pseudophilotes sinaicus (Lycaenidae) was studied. Potential habitat within its range was first located and then the quality of that habitat assessed. Degree of shelter, diversity of plant species, and resource area of an individual food plant (Thymus decussatus) all affected habitat quality and together were used to develop an index of habitat suitability applicable to each site. The butterfly's distribution was then studied within the identified network of suitable habitat patches: isolated patches with a small resource area were least likely to contain butterflies. Population size in a patch (as opposed merely to patch occupancy) was affected by resource area and the quality of habitat within that patch. Metapopulation processes and variation in habitat quality therefore appear to combine to describe the distribution of patches occupied by P. sinaicus and their population sizes. This finding provides insights into some of the processes operating on an endemic species throughout its geographical range and has important implications for the conservation of this rare butterfly.     

Butterfly oviposition preference is not related to larval performance on a polyploid herb

The preference–performance hypothesis predicts that female insects maximize their fitness by utilizing host plants which are associated with high larval performance. Still, studies with several insect species have failed to find a positive correlation between oviposition preference and larval performance. In the present study, we experimentally investigated the relationship between oviposition preferences and larval performance in the butterfly Anthocharis cardamines. Preferences were assessed using both cage experiments and field data on the proportion of host plant individuals utilized in natural populations. Larval performance was experimentally investigated using larvae descending from 419 oviposition events by 21 females on plants from 51 populations of two ploidy types of the perennial herb Cardamine pratensis. Neither ploidy type nor population identity influenced egg survival or larval development, but increased plant inflorescence size resulted in a larger final larval size. There was no correlation between female oviposition preference and egg survival or larval development under controlled conditions. Moreover, variation in larval performance among populations under controlled conditions was not correlated with the proportion of host plants utilized in the field. Lastly, first instar larvae added to plants rejected for oviposition by butterfly females during the preference experiment performed equally well as larvae growing on plants chosen for oviposition. The lack of a correlation between larval performance and oviposition preference for A. cardamines under both experimental and natural settings suggests that female host choice does not maximize the fitness of the individual offspring.     

Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host

Exotic plants may act as population sinks or evolutionary traps for native herbivores. The native butterfly Pieris oleracea lays eggs on garlic mustard, Alliaria petiolata, but larvae develop very poorly on this exotic invasive plant. We examined oviposition preference of individual females and larval performance of their offspring for individuals from one area where garlic mustard is well established and one where it is absent. These data were used to assess whether garlic mustard is being incorporated into or excluded from the diet. Females from the area without garlic mustard showed a wide range of preference, families had low larval survival on garlic mustard, and larval survivorship showed no correlation with mothers’ preferences. Females from the area with garlic mustard preferred it to the native host, and larval survivorship on garlic mustard was positively correlated with the mother’s preference. Individuals surviving on garlic mustard took longer to pupate and weighed >30% less compared to pupae reared on normal hosts. Our results suggest that where garlic mustard is well established P. oleracea may be adapting to this plant by both improved larval performance and increased adult female oviposition preference for it.     

Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes

In theory, selection favours predators that select prey in order to maximise reproductive success. We studied the association between preference and performance of the generalist predator Orius laevigatus with respect to two prey species: spider mites ( Tetranychus urticae ) and western flower thrips ( Frankliniella occidentalis ). Under ample prey supply, the predators had higher maximum reproductive success (measured as intrinsic population growth rate r ) on thrips than on spider mites; hence thrips represent a higher prey quality to the bugs. This was at odds with the observed preference of the predatory bug for plants (patches) with high densities of spider mites to plants with moderate densities of thrips in release-recapture experiments. Thus, prey quality does not suffice to explain the preference of predators for plants with prey. The quality of a patch as an oviposition site (i.e. the number of eggs produced on a patch per bug per day) also did not match preference patterns. Hence, patch preference was not correlated to prey quality or oviposition rate on prey patches. However, patch productivity, i.e. the total number of offspring surviving until adulthood that can be produced by one female on a patch, was correlated with preference. This was further tested by offering the predators a choice between plants with high densities of spider mites and plants with high densities of thrips in an independent set of release-recapture experiments. These two types of prey patches were found equivalent in terms of patch productivity. Indeed, the predators showed no preference for either of the two types of patches, which is in agreement with our predictions. This suggests that the predatory bugs select patches based on patch productivity rather than on prey quality or oviposition rate on a patch.     

Fitness costs of butterfly oviposition on a lethal non-native plant in a mixed native and non-native plant community

Non-native plants may be unpalatable or toxic, but have oviposition cues similar to native plants used by insects. The herbivore will then oviposit on the plant, but the offspring will be unable to develop. While such instances have been described previously, the fitness costs at the population level in the wild due to the presence of the lethal host have not been quantified, for this or other related systems. We quantified the fitness cost in the field for the native butterfly Pieris macdunnoughii in the presence of the non-native crucifer Thlaspi arvense, based on the spatial distributions of host plants, female butterflies and eggs in the habitat and the survival of the larvae in the wild. We found that 2.9 % of eggs were laid on T. arvense on average, with a survival probability of 0, yielding a calculated fitness cost of 3.0 % (95 % confidence interval 1.7–3.6 %) due to the presence of the non-native in the plant community. Survival probability to the pre-pupal stage for eggs laid on two native crucifers averaged 1.6 % over 2 years. The magnitude of the fitness cost will vary temporally and spatially as a function of the relative abundance of the non-native plant. We propose that the fine-scale spatial structure of the plant community relative to the butterflies’ dispersal ability, combined with the females’ broad habitat use, contributes to the fitness costs associated with the non-native plant and the resulting evolutionary trap.     

Effects of fragmentation of secondary broadleaf deciduous forests on populations of the near-threatened butterfly, Sasakia charonda (Lepidoptera, Nymphalidae), in central Japan

We examined the effects of fragmentation of secondary broadleaf deciduous forests (secondary forests) on populations of the near-threatened butterfly, Sasakia charonda, in central Japan. Regression analyses revealed that the number of overwintering larvae per host tree significantly increased when the area of secondary forest patches and the Isolation Index of the forest patch increased and the distance from secondary forest patches containing the focal host trees to the nearest secondary forest patch decreased. There was a significantly positive correlation between the number of overwintering larvae and the number of host trees in the neighborhood. The host trees were primarily distributed at the edges of secondary forests. From the results of the backward elimination method of multiple linear regression analysis, independent variables other than patch area were eliminated, and the standardized partial regression coefficient of the patch area was significant. This result suggested that a contiguous distribution of large secondary forest patches with many host trees is very important to conserving this butterfly species.     

Population level correlation between pre-alighting and post-alighting host plant preference in the Glanville fritillary butterfly

1. In many populations of the Glanville fritillary butterfly Melitaea cinxia, ovipositing females exhibit a post‐alighting preference for one of the potential host plant species available. The work reported here aimed to establish whether females with different post‐alighting preferences can discriminate between their host plant species prior to alighting, and whether pre‐alighting and post‐alighting preferences are correlated at the population level. 2. Alighting and oviposition events were recorded for groups of females from six populations in greenhouse and field experiments. 3. Landing frequencies did not change with experience, indicating that M. cinxia females did not learn from previous encounters with host plants. 4. Females from populations exhibiting post‐alighting preference searched efficiently for their host plants in the sense that they landed mainly on the species on which they oviposited predominantly. Pre‐alighting and post‐alighting preferences were correlated at the population level. 5. The correlation between pre‐alighting and post‐alighting preferences helps to explain why in nature, where the host plants often occur in distinct patches, females are more likely to colonise habitat patches in which their preferred host plant is abundant.     

Frequency Dependence of Host Plant Choice within and Between Patches: A Large Cage Experiment

Oviposition preference is considered to be one of the most important factors behind patterns of host use among herbivorous insects. However, preference is defined as host plant choice under equal host abundance and availability, and it is likely that frequency-dependent effects will alter the actual pattern of host use beyond what preference trials reveals. The effects of such alterations are poorly known but could be important for the understanding of specialization and host shifts. We investigated how changes in frequency of a preferred and a less preferred host affected movement patterns and egg deposition within and among patches in a polyphagous butterfly, Polygonia c-album. Two experiments were carried out in large (8 × 30 m) outdoor cages, artificially divided into distinct patches with different frequencies of the two hosts: one that allowed for limited movement between patches and one that did not. There was a clear effect of frequency on patch selection; females spent more time in and laid more eggs in patches with a high frequency of the preferred host, which will potentially have a large effect on host use by modifying encounter rates in favor of the preferred host. However, there was no significant frequency-dependent plant choice within patches in any experiment. Instead, results indicate that females are distributing their eggs among plants species according to specific likelihoods of oviposition, independent of encounter rates, which is compatible with a strategy of risk-spreading.Co-ordinating editor: N. Yamamura     

Taxonomic homogenization of woodland plant communities over 70 years

Taxonomic homogenization (TH) is the increasing similarity of the species composition of ecological communities over time. Such homogenization represents a form of biodiversity loss and can result from local species turnover. Evidence for TH is limited, reflecting a lack of suitable historical datasets, and previous analyses have generated contrasting conclusions. We present an analysis of woodland patches across a southern English county (Dorset) in which we quantified 70 years of change in the composition of vascular plant communities. We tested the hypotheses that over this time patches decreased in species richness, homogenized, or shifted towards novel communities. Although mean species richness at the patch scale did not change, we found increased similarity in species composition among woodlands over time. We concluded that the woodlands have undergone TH without experiencing declines in local diversity or shifts towards novel communities. Analysis of species characteristics suggested that these changes were not driven by non-native species invasions or climate change, but instead reflected reorganization of the native plant communities in response to eutrophication and increasingly shaded conditions. These analyses provide, to our knowledge, the first direct evidence of TH in the UK and highlight the potential importance of this phenomenon as a contributor to biodiversity loss.     

The role of pre- and post- alighting detection mechanisms in the responses to patch size by specialist herbivores

Experimental data on the relationship between plant patch size and population density of herbivores within fields often deviates from predictions of the theory of island biogeography and the resource concentration hypothesis. Here we argue that basic features of foraging behaviour can explain different responses of specialist herbivores to habitat heterogeneity. In a combination of field and simulation studies, we applied basic knowledge on the foraging strategies of three specialist herbivores: the cabbage aphid (Brevicoryne brassicae), the cabbage butterfly (Pieris rapae L.) and the diamondback moth (Plutella xylostella L.), to explain differences in their responses to small scale fragmentation of their habitat. In our field study, populations of the three species responded to different sizes of host plant patches (9 plants and 100 plants) in different ways. Densities of winged cabbage aphids were independent of patch size. Egg‐densities of the cabbage butterfly were higher in small than in large patches. Densities of diamondback moth adults were higher in large patches than in small patches. When patches in a background of barley were compared with those in grass, densities of the cabbage aphid and the diamondback moth were reduced, but not cabbage butterfly densities. To explore the role of foraging behaviour of herbivores on their response to patch size, a spatially explicit individual‐based simulation framework was used. The sensory abilities of the insects to detect and respond to contact, olfactory or visual cues were varied. Species with a post‐alighting host recognition behaviour (cabbage aphid) could only use contact cues from host plants encountered after landing. In contrast, species capable with a pre‐alighting recognition behaviour, based on visual (cabbage butterfly) or olfactory (diamondback moth) cues, were able to recognise a preferred host plant whilst in flight. These three searching modalities were studied by varying the in flight detection abilities, the displacement speed and the arrestment response to host plants by individuals. Simulated patch size – density relationships were similar to those observed in the field. The importance of pre‐ and post‐ alighting detection in the responses of herbivores to spatial heterogeneity of the habitat is discussed.     

VARIATION IN PREFERENCE AND SPECIFICITY IN MONOPHAGOUS AND OLIGOPHAGOUS SWALLOWTAIL BUTTERFLIES

Although variation in oviposition preference and specificity for host plants has been demonstrated within populations of a variety of oligophagous insect species, it is unknown whether genetic variation in host choice is lost within populations of monophagous species. Analysis of a locally monophagous butterfly species, Papilio oregonius, and a locally oligophagous species, P. zelicaon, showed significant variation in oviposition preference within populations of both species. Females of both species chose primarily their native hosts. Nonetheless, the percentages of eggs laid by individual females among the plant species and the number of plant species on which individual females laid eggs differed significantly among isofemale strains within populations. Moreover, some females within all isofemale strains of both species laid a few eggs on Foeniculum vulgare, an umbelliferous species that does not occur in the native habitats of these populations but is a host for Papilio species in other geographic areas. The results suggest that local monophagy and oligophagy in these species reflect the relative ranking among potential plant species. Both populations harbor variation in oviposition choice that could allow for host shifts if these populations invaded new habitats.