The effect of multi‐species host density on superparasitism and sex ratio in a gregarious parasitoid

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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.     

Rewiring of interactions in a changing environment: nettle-feeding butterflies and their parasitoids

Climate and land use change can alter the incidence and strength of biotic interactions, with important effects on the distribution, abundance and function of species. To assess the importance of these effects and their dynamics, studies quantifying how biotic interactions change in space and time are needed. We studied interactions between nettle-feeding butterflies and their shared natural enemies (parasitoids) locally and across 500 km latitudinal gradient in Sweden. We also examined the potential impact of the range-expansion of the butterfly Araschnia levana on resident butterflies via shared parasitoids, by studying how parasitism in resident butterflies covaries with the presence or absence of the newly-established species. We collected 6777 larvae of four nettle-feeding butterfly species (Aglais urticae, Aglais io, Ar. levana and Vanessa atalanta), over two years, at 19 sites distributed along the gradient. We documented the parasitoid complex for each butterfly species and measured their overlap, and analysed how parasitism rates were affected by butterfly species assemblage, variations in abundance, time, and the arrival of Ar. levana. Parasitoids caused high mortality, with substantial overlap in the complex of parasitoids associated with the four host butterflies. Levels of parasitism differed significantly among butterflies and were influenced by the local butterfly species assemblage. Our results also suggest that parasitism in resident butterflies is elevated at sites where Ar. levana has been established for a longer period. In our study system, variations in butterfly species assemblages were associated in a predictable way with substantial variations in rates of parasitism. This relationship is likely to affect the dynamics of the butterfly host species, and potentially cascade to the larger number of species with which they interact. These results highlight the importance of indirect interactions and their potential to reorganise ecological communities, especially in the context of shifts in species distributions in a warmer world.     

The roles of foraging environment,host species,and host diet for a generalist pupal parasitoid

Even for parasitoids with a wide host range, not all host species are equally suitable, and host quality often depends on the plant the host feeds on. We compared oviposition choice and offspring performance of a generalist pupal parasitoid, Pteromalus apum (Retzius) (Hymenoptera: Pteromalidae), on two congeneric hosts reared on two plant species under field and laboratory conditions. The plants contain defensive iridoid glycosides that are sequestered by the hosts. Sequestration at the pupal stage differed little between host species and, although the concentrations of iridoid glycosides in the two plant species differ, there was no effect of diet on the sequestration by host pupae. The rate of successful parasitism differed between host species, depending on the conditions they were presented in. In the field, where plant‐associated cues are present, the parasitoid used Melitaea cinxia (L.) over Melitaea athalia (Rottemburg) (Lepidoptera: Nymphalidae), whereas more M. athalia were parasitised in simplified laboratory conditions. In the field, brood size, which is partially determined by rate of superparasitism, depended on both host and plant species. There was little variation in other aspects of offspring performance related to host or plant species, indicating that the two host plants are of equal quality for the hosts, and the hosts are of equal quality for the parasitoids. Corresponding to this, we found no evidence for associative learning by the parasitoid based on their natal host, so with respect to these host species they are truly generalist in their foraging behaviour.     

Apparent competition leaves no detectable imprint on patterns of community composition: observations from a natural experiment

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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.     

Habitat exploration in butterflies – an outdoor cage experiment

A large outdoor cage, measuring 7 × 30 m, was used to study the willingness of butterflies to move through unsuitable habitat in search of neighbouring patches. The area inside the cage was divided into two grassland parts by a 7 m long shady part of unsuitable habitat that the butterflies had to fly through to move between the grassland parts. In 1999 and 2000 we performed experiments on three Melitaeini species (Melitaea cinxia and Mellicta athalia were used both years and Euphydryas aurinia in 2000) and three additional species (Brenthis ino and Aphantopus hyperantus in 1999 and Clossiana euphrosyne in 2000). In both years the Melitaeini species moved at considerably lower rates through the shady part than the other species. Among the Melitaeini species Mell. athalia moved most frequently through the shady part while E. aurinia and M. cinxia moved at lower rates. The distribution of these butterflies differ from widespread to localized and the results are discussed in the context of their habitat preferences and distribution patterns.     

Temporal and geographic variation in parasitoid attack with no evidence for ant protection of the Melissa blue butterfly,Lycaeides melissa

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Relative influences of plant type and parasitoid initial density on host–parasitoid relationships in a tritrophic system

To explore the effects of bottom-up and top-down forces on the relationships between a host, Plutella xylostella (L.) (Lepidoptera, Plutellidae), and its parasitoid, Cotesia vestalis (Haliday) (Hymenoptera, Braconidae), a short-term field experiment was established as a factorial experiment using three different host plants (Brassica pekinensis cv. Yuki F1, Brassica oleracea var. capitata cv. Midorimaru F1 and B. oleracea var. botrytis cv. Snow Crown) in the presence of C. vestalis at two different levels (low and high initial release). The tritrophic interactions were monitored by census counts of live adults 20?days after parasitoid release. The mean numbers of P. xylostella and C. vestalis adults were compared using log-linear analysis of deviance. Also, differences in the levels of parasitism were analysed using logistic analysis of deviance. There was a significant effect of host plant type on the abundance of P. xylostella, the abundance of C. vestalis and the percentage parasitism of P. xylostella by C. vestalis. The mean number of P. xylostella adults per cage on common cabbage or cauliflower was significantly greater than that on Chinese cabbage. The mean number of C. vestalis adults and the proportion of hosts attacked by C. vestalis per cage were significantly greater on Chinese cabbage compared with common cabbage or cauliflower. Indeed, initial parasitoid release did not significantly affect the abundance of P. xylostella but there was a significant influence of initial parasitoid release on the abundance of C. vestalis and the levels of parasitism of P. xylostella by C. vestalis. The mean number of C. vestalis adults and the proportion of P. xylostella parasitised by C. vestalis per cage were greater in high level of parasitoid release compared with low level of parasitoid release. However, there were no significant interacting effect of the factors (plant type?×?parasitoid initial abundance) on the abundance of P. xylostella, the population size of C. vestalis and parasitism of P. xylostella by C. vestalis.     

Habitat utilization of the Glanville fritillary butterfly in the Tianshan Mountains, China, and its implication for conservation

In 2004 and 2005, we investigated the distribution of the Glanville fritillary butterfly (Melitaea cinxia) and its host plant in the Tianshan Mountains of China, in order to clarify its habitat utilization. Female butterflies were almost captured on dry meadows on slopes, where plenty of host plant (Veronica spicata) is distributed. Although there are host plants on meadows at higher altitude (>2,050 m), no butterfly was found there. Among the meadows with host plants, a patch of dry meadow (newly-found meadow) was considered as a natal site because of the high density and freshness of butterflies. Unlike females, male butterflies were almost captured in valleys, where there are no host plants and fewer nectar plants. It might be related to specific mating system of M. cinxia in the study site, or specific environmental factors. Thus valleys are important habitat for males. Although the status of M. cinxia is yet unknown in China, we give some suggestions for conservation based on this study. First, dry meadows with host plants are the essential component for persistence of M. cinxia, among which the specific sites with more favourable conditions, such as natal site, are most important. Second, as a site with adult resource requirement, valleys should be included as part of the habitat of the butterfly. Finally, meadows at higher altitude are not utilized at present but they are potential habitats which need to be maintained for any shifts in altitudinal range in response to global warming in the future. Hence, the trade-off of present cost and future benefit should be taken into account when formulating a conservation strategy for M. cinxia in the Tianshan Mountains of China.     

N equals two (times five). Exploring the effects of horse rewilding on five congeneric adult butterflies

Rewilding incomplete ecosystems by using ungulate megaherbivores represents a significant potential for sustainable management of habitats of declining species. Two xeric grasslands patches in the Podyjí National Park, Czech Republic, were rewilded by a feral horse breed, the Exmoor pony, in 2018. Before this in 2017, demography, mobility, and adult habitat use of five congeneric Melitaea butterflies co-occurring at the grasslands were investigated (Vodickova et al., J. Nature Conserv. 2019). In 2021, four seasons after the rewilding, we replicated the survey to assess the effects of the horse on the butterflies. Here, we compare the results of the two surveys and investigate changes in spatial patterns of adult distribution using Ripley’s K-functions.Total numbers of captures, and estimated population sizes, were consistently lower in 2021, with the largest drop for spring-flying M. cinxia. We cannot discern whether this was due to the cold 2021 spring, or due to reduction of grasses by the horse, possibly contributing to desiccation of M. cinxia host plants. Demographic parameters such as residency/longevity and capture probability changed only little. Mobility ranking among species remained identical, but within species, some mobility characteristics changed among years. Among early summer species, M. britomartis, second most abundant in 2017, switched to the first position with M. aurelia, and these two species displayed the most notable shift in adult habitat use between the two seasons. Short thorny shrubs avoided by the horse protect M. britomartis host plants; this threatened butterfly thus did not suffer from horse presence. M. athalia, a species of woodland edges, profited from decay of conifers caused by a series of dry years; and M. didyma, forming multiple generations, from increase of its host plant. Contrary to expectations, spatial distribution of most butterflies became more aggregated within rewilded pastures, probably due to regularities in home ranges use by the horses, which restructured the vegetation in a zonal, rather than patchy, way. A considerably larger areas should be rewilded by the herbivores to fully achieve the desired beneficial effects.     

Parabiotic ants: the costs and benefits of symbiosis

1. Mutualisms are important drivers of co‐evolution and speciation. However, they typically imply costs for one or both partners. Each partner consequently tries to maximise benefits and minimise costs. Mutualisms can therefore develop towards commensalism or parasitism if one partner fails to provide sufficient benefits. This is particularly likely in diffuse interactions, where multiple species can associate with each other. If costs and benefits of a species vary with the identity of the partner species, this may result in a geographical mosaic of co‐evolution. 2. In the present study, inter‐specific interactions in two parabiotic associations of ants were studied (Hymenoptera: Formicidae). One Crematogaster species was associated with one of two closely related Camponotus species. We assessed cost and benefits by studying behavioural interactions, foraging behaviour, and nest defence in the associations. 3. While parabioses had been shown to be mutualistic, evidence was found for exploitation and aggressive competition between species. In spite of apparent costs of being exploited, we found no benefits for one partner (Crematogaster). The magnitude of potential costs to Crematogaster varied between the two Camponotus species. 4. We conclude that the cost/benefit ratio for Crematogaster varies between the two Camponotus partners, and between environmental conditions. Parabiosis can thus fluctuate between mutualism, commensalism, and parasitism, with Crematogaster being the species that may have higher costs than benefits. 5. We suggest that geneflow in the Crematogaster population hinders local adaptation to the resulting mosaic of locally varying selection pressures. This study demonstrates how diffuse interactions and environmental variation can result in a complex of local selection pressures.     

The impact of habitat fragmentation on trophic interactions of the monophagous butterfly <Emphasis Type="Italic">Polyommatus coridon</Emphasis>

Theory predicts that habitat fragmentation, including reduced area and connectivity of suitable habitat, changes multitrophic interactions. Species at the bottom of trophic cascades (host plants) are expected to be less negatively affected than higher trophic levels, such as herbivores and their parasitoids or predators. Here we test this hypothesis regarding the effects of habitat area and connectivity in a trophic system with three levels: first with the population size of the larval food plant Hippocrepis comosa, next with the population density of the monophagous butterfly species Polyommatus coridon and finally with its larval parasitism rate. Our results show no evidence for negative effects of habitat fragmentation on the food plant or on parasitism rates, but population density of adult P. coridon was reduced with decreasing connectivity. We conclude that the highly specialized butterfly species is more affected by habitat fragmentation than its larval food plant because of its higher trophic position. However, the butterfly host species was also more affected than its parasitoids, presumably because of lower resource specialization of local parasitoids which also frequently occur in alternative hosts. Therefore, conservation efforts should focus first on the most specialized species of interaction networks and second on higher trophic levels.     

Multitrophic interactions drive body size variations in seed-feeding insects

1. The intensity of community interactions and the structure of food webs can be associated with an organism's body size. However, little is known about how interactions among species in multitrophic communities determine the body size of individuals exploiting the same resource. 2. This study evaluates the effects of resource size, fruit infestation, and parasitism on tibia length, a proxy measure of body size, of insects exploiting the same resource. The three most abundant seed-feeding species of Senegalia tenuifolia (Fabaceae: Mimosoideae) were selected, and the relationship between their tibia length and the interactions within the food web was estimated. The selected species were the beetles Merobruchus terani and Stator maculatopygus, and the braconid wasp Allorhogas vulgaris. 3. The body sizes of 531 specimens were measured and it was found that tibia length of each species responded differently to the interactions, demonstrating that functionally similar species may respond differently to multitrophic effects. The body size of Merobruchus terani, the most abundant species in the food web, was negatively affected by the presence of A. vulgaris, but there was a positive relationship with seed biomass and its own abundance in the fruits. The other two species were less abundant and more plastic in their responses, as a strong negative effect of M. terani presence on A. vulgaris body size was observed, as well as a strong negative effect of Coleoptera parasitism rate on S. maculatopygus body size. 4. It is concluded that morphological traits can provide information on how interactions affect species body size.     

Do distances among host patches and host density affect the distribution of a specialist parasitoid?

The effect of spatial habitat structure and patchiness may differ among species within a multi-trophic system. Theoretical models predict that species at higher trophic levels are more negatively affected by fragmentation than are their hosts or preys. The absence or presence of the higher trophic level, in turn, can affect the population dynamics of lower levels and even the stability of the trophic system as a whole. The present study examines different effects of spatial habitat structure with two field experiments, using as model system the parasitoid Cotesia popularis which is a specialist larval parasitoid of the herbivore Tyria jacobaeae. One experiment examines the colonisation rate of the parasitoid and the percentage parasitism at distances occurring on a natural scale; the other experiment examines the dispersal rate and the percentage parasitism in relation to the density of the herbivore and its host plant. C. popularis was able to reach artificial host populations at distances up to the largest distance created (at least 80 m from the nearest source population). Also, the percentage parasitism did not differ among the distances. The density experiment showed that the total number of herbivores parasitised was higher in patches with a high density of hosts, regardless of the density of the host plant. The percentage parasitism, however, was not related to the density of the host. The density of the host plant did have a (marginally) significant effect on the percentage parasitism, probably indicating that the parasitoid uses the host plant of the herbivore as a cue to find the herbivore itself. In conclusion, the parasitoid was not affected by the spatial habitat structure on spatial scales that are typical of local patches.     

Parasitism as a biological control agent of dinoflagellate blooms in the California Current System

Amoebophrya is a marine parasite recently found to infect and kill bloom-forming dinoflagellates in the California Current System (CCS). However, it is unknown whether parasitism by Amoebophrya can control dinoflagellate blooms in major eastern boundary upwelling systems, such as the CCS. We quantified the abundance of a common bloom-forming species Akashiwo sanguinea and prevalence of its parasite (i.e., % infected cells) in surface water samples collected weekly from August 2005 to December 2008 at the Santa Cruz Wharf (SCW), Monterey Bay, CA. Additionally, we measured physical and chemical properties at the SCW and examined regional patterns of wind forcing and sea surface temperature. Relative abundance of the net phytoplankton species was also analyzed to discern whether or not parasitism influences net phytoplankton community composition. Epidemic infection outbreaks (>20% parasite prevalence in the host species) may have contributed to the end or prevented the occurrence of A. sanguinea blooms, whereas low parasite prevalence was associated with short-term (≤2 weeks) A. sanguinea blooms. The complete absence of parasitism in 2007 was associated with an extreme A. sanguinea bloom. Anomalously strong upwelling conditions were detected in 2007, suggesting that A. sanguinea was able to outgrow Amoebophrya and ‘escape’ parasitism. We conclude that parasitism can strongly influence dinoflagellate bloom dynamics in upwelling systems. Moreover, Amoebophrya may indirectly influence net phytoplankton species composition, as species that dominated the net phytoplankton and developed algal blooms never appeared to be infected.     

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.     

Metapopulation dynamics in a changing climate: Increasing spatial synchrony in weather conditions drives metapopulation synchrony of a butterfly inhabiting a fragmented landscape

Habitat fragmentation and climate change are both prominent manifestations of global change, but there is little knowledge on the specific mechanisms of how climate change may modify the effects of habitat fragmentation, for example, by altering dynamics of spatially structured populations. The long‐term viability of metapopulations is dependent on independent dynamics of local populations, because it mitigates fluctuations in the size of the metapopulation as a whole. Metapopulation viability will be compromised if climate change increases spatial synchrony in weather conditions associated with population growth rates. We studied a recently reported increase in metapopulation synchrony of the Glanville fritillary butterfly (Melitaea cinxia) in the Finnish archipelago, to see if it could be explained by an increase in synchrony of weather conditions. For this, we used 23 years of butterfly survey data together with monthly weather records for the same period. We first examined the associations between population growth rates within different regions of the metapopulation and weather conditions during different life‐history stages of the butterfly. We then examined the association between the trends in the synchrony of the weather conditions and the synchrony of the butterfly metapopulation dynamics. We found that precipitation from spring to late summer are associated with the M. cinxia per capita growth rate, with early summer conditions being most important. We further found that the increase in metapopulation synchrony is paralleled by an increase in the synchrony of weather conditions. Alternative explanations for spatial synchrony, such as increased dispersal or trophic interactions with a specialist parasitoid, did not show paralleled trends and are not supported. The climate driven increase in M. cinxia metapopulation synchrony suggests that climate change can increase extinction risk of spatially structured populations living in fragmented landscapes by altering their dynamics.     

Spatial patterns of host exploitation in a larval parasitoid of the predatory dusky large blue Maculinea nausithous

The foraging behaviour of the parasitoid wasp Neotypus melanocephalus and factors affecting parasitism at the population level were studied. This specialised parasitoid attacks caterpillars of the butterfly Maculinea nausithous, which sequentially feed on the plant Sanguisorba officinalis and specific red Myrmica ants. Among M. nausithous populations, there is considerable variation in caterpillar densities. At low M. nausithous densities, foraging might be time consuming for N. melanocephalus. High host densities may not always be advantageous to foraging parasitoids due to the caterpillars’ frequent overexploitation of ant resources and subsequent density-dependent mortality. In order to disperse progeny, we hypothesised that N. melanocephalus should search in a non-random way at the level of the micro-habitat, i.e., single flower heads of S. officinalis. Our analysis of 32 natural populations in the Upper Rhine valley in Germany did not show a density-dependent relationship between M. nausithous caterpillars and parasitism. Furthermore, habitat parameters like patch size and density of the host's food plant did not affect the parasitism rate. Foraging N. melanocephalus females preferred to search on large flower heads. They probed host-occupied flower heads only, visiting non-host-exploited flower heads only briefly. Time spent on a flower head was independent of the number of caterpillars per flower head. This study indicates that N. melanocephalus increases its foraging efficiency by preferring large flower heads that were previously shown to contain more host caterpillars than small flower heads. Furthermore, oviposition increases the likelihood of continuing to search on a flower head, which is an adaptive strategy for parasitoids foraging for aggregated hosts. However, many host-occupied flower heads were not probed by N. melanocephalus. We discuss the possibility that temporal host refuges of M. nausithous caterpillars might contribute to heterogeneity of parasitism, and why spreading offspring might constitute a suitable strategy for a parasitoid of an ant-parasitic butterfly.