Differential Bird Predator Attack Rate on Seasonal Forms of the Map Butterfly (Araschnia levana L.): Does the Substrate Matter?

The European map butterfly (Araschnia levana L.) is a striking example of seasonal plasticity. Individuals of the spring generation are reddish with a fritillary‐like colour pattern, whereas the summer generation is black with a white dorsal stripe. Proximate factors explaining the development of the forms are well known, but ultimate explanations have not been tested experimentally yet. The reddish spring form is assumed to have a warning coloration, as found in other nymphalid butterflies that are unpalatable (Aglais urticae). We tested for differential predation by a visually hunting predator (Parus major) in a laboratory experiment using artificial butterflies designed to represent the spring and summer form. Birds were released individually in a flight cage where the alternative forms were presented. Summer forms were more frequently attacked than spring forms, which may point to some aversion against the reddish spring form. But there was also a strong effect of the interaction between seasonal form and type of substrate. Spring forms were much better protected from attacks on the brown substrate of dead leaves compared to the green substrate of nettle leaves. On the latter substrate, latency times before attacking spring forms were on average 2.5 times longer than for summer forms. Experiments with artificial butterflies simplify complex predator–prey interactions because they exclude potential taste or odour effects and they also exclude behavioural responses and interactions of the butterfly. However, our results based on static visual signals provide a promising first step to test the functional significance of this striking seasonal polyphenism.     

Allee effects and population regulation: a test for biotic resistance against an invasive leafroller by resident parasitoids

Resident natural enemies can impact invasive species by causing Allee effects, leading to a reduction in establishment success of small founder populations, or by regulating or merely suppressing the abundance of established populations. Epiphyas postvittana, the Light Brown Apple Moth, an invasive leafroller in California, has been found to be attacked by a large assemblage of resident parasitoids that cause relatively high rates of parasitism. Over a 4-year period, we measured the abundance and per capita growth rates of four E. postvittana populations in California and determined parasitism rates. We found that at two of the sites, parasitism caused a component Allee effect, a reduction in individual survivorship at lower E. postvittana population densities, although it did not translate into a demographic Allee effect, an impact on per capita population growth rates at low densities. Instead, E. postvittana populations at all four sites exhibited strong compensatory density feedback throughout the entire range of densities observed at each site. As we found no evidence for a negative relationship between per capita population growth rates and parasitism rates, we concluded that resident parasitoids were unable to regulate E. postvittana populations in California. Despite a lack of evidence for regulation or a demographic Allee effect, the impact of resident parasitoids on E. postvittana populations is substantial and demonstrates significant biotic resistance against this new invader.     

A novel parasitoid and a declining butterfly: cause or coincidence?

1. The small tortoiseshell butterfly (Aglais urticae L.) is considered to be a widespread and abundant generalist species in Northern Europe. However, it declined sharply in the U.K. between 2003 and 2008, coinciding with the arrival and spread of a parasitoid, Sturmia bella Meig. (Diptera: Tachinidae), which specialises on nymphalid butterflies. 2. Whether the decline in A. urticae is associated with the arrival of S. bella was investigated using data from a large‐scale butterfly monitoring scheme, and by collecting larvae to assess parasitoid incidence and parasitism frequency. Similar data were compiled for a related butterfly (Inachis io) which is also parasitised by S. bella but which is not declining. 3. Sturmia bella was recorded as far north as north Lincolnshire (53.53°N). Aglais urticae has declined significantly to the south of this latitude, but not to the north. 4. Sturmia bella was present in 26% and 15% of the larval groups of A. urticae and I. io, respectively, and now kills more individuals of A. urticae (but not I. io) than any native parasitoid. 5. Survival was 25–48% lower in batches of A. urticae larvae where S. bella was present, indicating that S. bella causes host mortality in addition to that caused by native parasitoids. 6. Our results suggest that S. bella may be playing a role in the recent decline of A. urticae. However, further research is needed to establish its effects relative to other potential drivers of trends in the abundance of this butterfly.     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

Maternal body size as a morphological constraint on egg size and fecundity in butterflies

It is a widespread notion that in arthropods female reproductive output is strongly affected by female size. In butterflies egg size scales positively with female size across species, suggesting a constraint imposed by maternal size. However, in intraspecific comparisons body size often explains only a minor part of the variation in progeny size. We here include representatives of various butterfly families to test the generality of this phenomenon across butterflies. Phenotypic correlations between egg and maternal body size were inconsistent across species: correlations were non-significant for Pararge aegeria and Lycaena tityrus, significantly positive for Papilio machaon, significantly negative for Araschnia levana, and contradictory for Pieris napi. Thus, there was no general pattern linking egg size to maternal size, e.g., caused by an allometric relationship. Consequently, there was at best limited evidence for maternal size acting as a morphological constraint on egg size within butterfly species. Realized fecundity depended on maternal size in P. napi and A. levana, but not in P. aegeria, suggesting that maternal size may affect egg number more strongly than egg size. Yet, variation in fecundity was primarily explained by variation in longevity as is expected for income breeders. Heritability estimates across species were rather similar for pupal mass (ranging between 0.14 and 0.19), but more variable for egg size (0.17–0.31).     

Parasitism rate of Plebejus argyrognomon (Lepidoptera: Lycaenidae) under different levels of mowing management

Plebejus argyrognomon is an endangered grassland butterfly species in Japan. In this study we focused on the parasitism rate of tachinid flies under different mowing management to obtain knowledge of this possible top-down effect that has been largely ignored. We established three mowing treatments differing in the intensity of mowing, as represented by vegetation height. The results showed that the parasitism rate of P. argyrognomon increased with vegetation height; the parasitism rate in blocks subjected to the highest mowing intensity was 8%, whereas in blocks subjected to the lowest mowing intensity, the rate was 42%. We suggest that clarifying interspecific interactions is important for understanding how habitat management affects grassland-inhabiting butterflies in general.     

Indirect interaction between butterfly species mediated by a shared pupal parasitoid

Indirect interactions among species can greatly affect their abundances and the structure of the community they live in. Using a field experiment, we tested the hypothesis that congeneric butterfly species interact indirectly through a shared pupal parasitoid. We predicted that symmetrical apparent competition would lead to high parasitism of both species, and the effect would increase with regional butterfly abundance. Instead, parasitism of one host, Melitaea cinxia, was reduced in the presence of the second host, M. athalia. Parasitism of M. athalia did not differ whether or not M. cinxia was present. This pattern did not vary with regional butterfly abundance, though overall rate of parasitism did. Details of the experiment suggest that the apparent commensalism occurred because M. cinxia pupae are protected by silk tents whereas M. athalia are exposed, causing locally foraging parasitoids to favour the more accessible host where the two are present together. The local short-term apparent commensalism favouring M. cinxia opposes the landscape scale trend, in which parasitism increases where butterfly density is high. The outcome of this study illustrates short-term apparent commensalism, that host suitability can depend on relative accessibility, and that indirect interactions occurring at different scales may be in opposition.     

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.     

Comparative food web structure of larval macrolepidoptera and their parasitoids on two riparian tree species

Single species or groups of species can be subjected to differing levels of parasitism on different plants. Previous studies have reported that parasitism of larval macrolepidoptera in an assemblage on box elder (Acer negundo L.) was significantly greater than on black willow [Salix nigra (Marsh)]. In this study, quantitative food webs, parasitoid overlap diagrams and other food web attributes were used to identify and describe direct and indirect interactions, and to compare assemblages on each tree species. These comparisons helped identify possible mechanisms explaining the differential parasitism observed. Although links among numerically dominant species in each assemblage were not strong, links between numerically dominant and subdominant species were strong. That is, numerically dominant and subdominant species interacted via shared parasitoids. The degree of parasitoid sharing by numerically dominant and subdominant species differed in each tree. There was less sharing of parasitoids on black willow than on box elder. Further, on box elder, the majority of parasitoids affecting numerically subdominant species originated from numerically dominant species, unlike in willow. These results lead to a working hypothesis—the source/nursery hypothesis—that proposes that community-wide levels of parasitism are highest in circumstances in which numerically subdominant species share parasitoid species in common with numerically dominant species, and most parasitoids attacking subdominant species originate from numerically dominant species. Thus, differences in degree of sharing and the types of herbivores sharing parasitoids may explain differential parasitism. Further, the source/nursery hypothesis may explain why the vast majority of species in most assemblages are numerically subdominant. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Lack of enemy release for an invasive leafroller in California: temporal patterns and influence of host plant origin

The enemy release hypothesis posits that the success of invasive species can be attributed to their escape from natural enemies. Invading hosts are expected to encounter an enemy assemblage consisting of fewer species, with lower representation of specialists, and to experience less mortality as a result. In this study, we examined parasitism of the Light Brown Apple Moth (LBAM), Epiphyas postvittana (Walker), in California, an exotic leafroller that is native to southeastern Australia. From 2008 to 2011 we monitored parasitoid species richness, representation of the more specialized koinobiont parasitoids, and parasitism rates of LBAM collected three times per year from four plant species of Australian origin and six plant species of non-Australian origin, at two locations in coastal California. We found the resident parasitoid assemblage of LBAM in California to have comparable levels of species richness, to have a similar representation of koinobionts versus idiobionts, and to inflict similar parasitism rates as in its native range. The two dominant parasitoids were Meteorus ictericus (Braconidae) and Enytus eureka (Ichneumonidae). Parasitoid species richness varied with season and plant origin and decreased slowly, but significantly, over the 4 year period. Parasitism rates were lowest in spring and highest on plants of Australian origin, but did not change with year. Hyperparasitism rates were higher on E. eureka (36.5 %) compared with M. ictericus and other parasitoids combined (3.3 %) and were highest on plants of Australian origin. We subsequently discuss the lack of both apparent enemy reduction and realized enemy release for LBAM in California and the unique finding that a shared plant origin enhanced the parasitism of this exotic leafroller by resident parasitoids.     

Plant Fertilization Interacts with Life History: Variation in Stoichiometry and Performance in Nettle-Feeding Butterflies

Variation in food stoichiometry affects individual performance and population dynamics, but it is also likely that species with different life histories should differ in their sensitivity to food stoichiometry. To address this question, we investigated the ability of the three nettle-feeding butterflies (Aglais urticae, Polygonia c-album, and Aglais io) to respond adaptively to induced variation in plant stoichiometry in terms of larval performance. We hypothesized that variation in larval performance between plant fertilization treatments should be functionally linked to species differences in host plant specificity. We found species-specific differences in larval performance between plant fertilization treatments that could not be explained by nutrient limitation. We showed a clear evidence of a positive correlation between food stoichiometry and development time to pupal stage and pupal mass in A. urticae. The other two species showed a more complex response. Our results partly supported our prediction that host plant specificity affects larval sensitivity to food stoichiometry. However, we suggest that most of the differences observed may instead be explained by differences in voltinism (number of generations per year). We believe that the potential of some species to respond adaptively to variation in plant nutrient content needs further attention in the face of increased eutrophication due to nutrient leakage from human activities.     

Beneath the bark: associations among Sirex noctilio development,bluestain fungi,and pine host species in North America

1. Invasive species with global distributions encounter unique environmental and biotic variables that can greatly affect the magnitude of their impact. The European woodwasp, Sirex noctilio Fabricius, is a prime example that has invaded climatically and ecologically distinct ecosystems across the Southern Hemisphere and, more recently, North America. 2. Northeastern North America presents a unique set of conditions, including pine host species, native parasitoids, a diverse assemblage of native co‐colonising insects, and fungal associates of these co‐colonisers. In North America, S. noctilio attacks both a naturalised ancestral host (Pinus sylvestris L.) from Europe and a naïve native host (P. resinosa). A large assemblage of insects and their associated bluestaining ophiostomatoid fungi colonise these pines. Competition between S. noctilio and this group is a hypothesised mechanism of biotic resistance in the invaded region of North America, possibly via superior resource capture abilities or alteration of host tissue by bluestain fungi. 3. Investigating these ecological interactions is challenging because they manifest deep in the xylem tissue. To overcome this, 30 experimentally stressed trees were systematically dissected with an electric log splitter to investigate the effects of bluestain fungi and tree factors on S. noctilio development and parasitism by native hymenopterans. 4. Body size and colonisation density were affected by pine species, with S. noctilio being 25% larger and densities three‐fold greater in P. sylvestris than P. resinosa. Survivorship was slightly negatively correlated with the proportional volume of bluestain infection. Interestingly, rhyssine (Rhyssa and Megarhyssa spp.) parasitism responded positively to greater S. noctilio density, but there was no density relationship with Ibalia leucospoides ensiger parasitism. Pine host species appears to play a strong role in S. noctilio development, which is important considering uninvaded regions of North America have a diversity of pine species that likely vary in their susceptibility to this woodborer.     

Response of native parasitoids to a range-expanding host

Abstract 1. As species shift their geographic distributions, new feeding interactions with natural enemies such as parasitoids, and resources such as host plants, may be established, and existing interactions may be severed. 2. The leaf mining moth Phyllonorycter leucographella (Zeller, 1850) (Lep.: Gracillariidae) first colonised the southern United Kingdom in the mid 1980s associated with its ancestral host plant Pyracantha coccinea M. Roem. (Rosaceae), which is widely cultivated in the U.K. The moth has since spread northwards to central Scotland and has been recorded feeding on a novel host plant, Crataegus monogyna L. 3. The combined effects of latitude and time since colonisation on parasitoid community responses to the arrival of this novel host were investigated across its U.K. range. The response of parasitoids to colonisation of C. monogyna was also investigated. 4. Both the observed richness of parasitoid species associated with P. leucographella, and the proportion of P. leucographella parasitised declined with latitude and towards the current range margin. A combination of a latitudinal gradient in parasitoid and alternative host species richness is likely to lead to the trends in species richness and parasitism observed. 5. Experimental host patches exposed to parasitism beyond the current range margin of P. leucographella experienced low levels of parasitism consistent with range‐margin populations, indicating an instantaneous response by native parasitoids to availability of the novel host. Parasitism levels and numbers of associated species in the U.K. were similar to those observed in the species’ native range in Turkey. 6. The host plant switch to C. monogyna was not associated with an altered parasitoid assemblage, but rates of parasitism were significantly higher on the novel host plant. 7. Alterations in the incidence and frequency of victim‐enemy interactions as species shift their geographic ranges may be key in determining rates of range expansion and the impact invading species have on ecological communities.     

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

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The biology of two Eretmocerus spp. (Haldeman) and three Encarsia spp. Forster and their potential as biological control agents of Bemisia tabaci biotype B in Australia

The performance, as measured by daily rate of parasitism and total parasitism, of five aphelinid species found in Australia parasitising Bemisia tabaci were compared on cotton, hibiscus, rockmelon, soybean and tomato. Two Eretmocerusspp., both indigenous to Australia, gave the highest levels of parasitism on each of the plant host species tested. The tritrophic interactions between B. tabaci, host plant species and Eret. mundus(Australian parthenogenetic form) (APF) were also examined. In general, more whiteflies were parasitised when cotton was the source host or rockmelon the test host. Parasitism was always low when tomato was either the source or test host. When parasitoids were transferred from rockmelon to cotton, parasitism declined. In contrast, parasitism increased when parasitoids were transferred from cotton to rockmelon. Parasitism also increased when parasitoids were transferred from soybean to rockmelon, yet failed to do so when shifted from soybean to cotton despite cotton normally being a better host. However, when parasitoids were transferred from cotton to soybean there was a marked increase in parasitism. Possible causes are discussed. The field cage trial demonstrated that parasitism by both Eretmocerus spp. increased with increasing whitefly density. Further, the increase in parasitism was not due to the presence of more parasitoids as neither the parasitoid-whitefly ratio nor the total number of parasitoids present had a significant effect on parasitism. The combination of the two species, gave similar levels of parasitism to that achieved by Eret. mundus(APF) alone. Subsequent identification of the emerged individuals indicated that over 50% of the parasitism was due to this species suggesting that it out-competed Eret. queenslandensis. Despite this competition, there was no evidence that overall control was compromised.     

Does Müllerian Mimicry Work in Nature? Experiments with Butterflies and Birds (Tyrannidae)1

The selective advantage of Müllerian mimicry in nature was investigated by releasing live mimetic and nonmimetic butterflies close to wild, aerial‐hunting tropical kingbirds (Tyrannus melancholicus) and cliff‐flycatchers (Hirundinea ferruginea) in three Amazon habitats (rain forest, a city, and “canga” vegetation). Only mimetic butterflies elicited sight‐rejections by birds, but protection conferred by mimicry was restricted to sites in which both predators and mimics co‐occurred, as in the case of six mimicry rings at a forest site and two at a city site. Most other Müllerian mimics released at city and canga vegetation were heavily attacked and consumed by birds. These results appear to reflect the birds’previous experiences with resident butterfly faunas and illustrate how birds’discriminatory behavior varied among habitats that differed in butterfly species and mimicry ring composition.     

Seasonal phenology and stage-specific parasitism of the apple ermine moth, Yponomeuta malinellus Zeller, in Korea

The apple ermine moth, Yponomeuta malinellus Zeller (Lepidoptera: Yponomeutidae), is a tent caterpillar that feeds on Malus spp. in Korea. Populations of the moth in native areas appeared to be regulated by the assemblage of parasitoids. Phenological associations between host stages and parasitoids, susceptible stage(s) of the host for each parasitoid, and stage‐specific parasitism were studied. The egg larval parasitoid Ageniaspis fuscicollis (Dalman) had highest parasitism of first instar larvae (24%), with 14% parasitism of other larval stages. Dolichogenidea delecta (Haliday) was recovered from all larval instars with the highest parasitism rate of second instar larvae (20.1%), followed by 19.9% parasitism of mid‐larval hosts. Herpestomus brunicornis Gravenhorst was reared from second instar larvae through to pupal collection, and had the highest parasitism rate (29.9%) at the pupal stage. The larval pupal parasitoid Zenillia dolosa (Meigen) was recovered from mid‐larval to pupal stages with the highest parasitism rate (5.5%) occurring in third to fourth instar larvae. The host stages for developing A. fuscicollis completely overlap with those of D. delecta, and with those of H. brunicornis to some degree. A statistically significant negative correlation exists between A. fuscicollis and these dominant parasitoids, indicating competitive interaction within the host.     

Seasonal changes in seaweed deposition,seaweed fly abundance,and parasitism at the pupal stage along sandy beaches in central Japan

Seasonal relationships among stranded wrack quantity, seaweed fly abundances, and parasitism at the pupal stage were studied along three sandy beaches in central Japan. The seasonal occurrence patterns of puparia of seaweed flies Coelopa frigida and Fucellia spp. generally corresponded to seaweed deposition, which peaked in May–July and October–December. Parasitoids use fly puparia in these seasons. However, the occurrence of seaweed flies and their parasitoids varied among the three sandy beaches and did not correspond to the wrack amounts. These findings suggest that populations of seaweed flies and their parasitoids are seasonally, but not spatially, regulated by bottom‐up processes. The parasitoid assemblage of fly puparia was composed of two Aleochara (Coleoptera: Staphylinidae), two Trichopria (Hymenoptera: Diapriidae), and five pteromalid species (Hymenoptera), but the rate of parasitism was less than 20% and might have had little effect on fly populations.     

The role of parasitoids in evolution of habitat and larval food plant preference by three Pieris butterflies

This article attempts to explain that parasitoids provide the evolutionary pressure responsible for relationships between habitat use and larval food plant use in herbivorous insects. Three species of butterflies of the genus Pieris, P. rapae, P. melete, and P. napi use different sets of cruciferous plants. They prefer different habitats composed of similar sets of cruciferous plants. In our study, P. rapae used temporary habitats with ephemeral plants, P. melete used permanent habitat with persistent plants, although they also used temporary habitats, and P. napi used only permanent habitat. The choice experiment in the field cages indicated that each of the three butterfly species avoided oviposition on plants usually unused in its own habitat, but accepted the unused plants which grew outside its own habitat. Their habitat use and plant use were not explained by intrinsic plant quality examined in terms of larval performance. Pieris larvae collected from persistent plants or more long lasting habitats were more heavily parasitized by two specialist parasitoids, the braconid wasp Cotesia glomerata and the tachinid fly Epicampocera succincta. The results suggest that Pieris habitat and larval food plant use patterns can be explained by two principles. The evolution of habitat preference may have been driven by various factors including escape from parasitism. Once habitat preference has evolved, selection favors the evolution of larval food plant preferences by discriminating against unsuitable plants, including those which are associated with high parasitism pressures. Received: December 3, 1998 / Accepted: January 20, 1999     

The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects

Seasonal polyphenism in animal colour patterns indicates that temporal variation in selection pressures maintains phenotypic plasticity. Spring generation of the polyphenic European map butterfly Araschnia levana has an orange–black fritillary‐like pattern whilst individuals of the summer generation are black with white bands across the wings. What selects for the colour difference is unknown. Because predation is a major selection pressure for insect coloration, we first tested whether map butterfly coloration could have a warning function (i.e. whether the butterflies are unpalatable to birds). In a following field experiment with butterfly dummies we tested whether the spring form is better protected than the summer form from predators in the spring, and vice versa in the summer. The butterflies were palatable to birds (blue tits Cyanistes caeruleus) and in the field the spring and summer form dummies were attacked equally irrespective of season. Therefore, we found no evidence that the map butterfly is warning‐coloured or that seasonal polyphenism is an adaptation to avian predation. Because insect coloration has multiple functions and map butterfly coloration is linked to morphology, life history and development it is likely that the interplay of several selection pressures explains the evolution of colour polyphenism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.