Coexistence of competing parasitoids: which is the fugitive and where does it hide?

Most insects harbour a community of parasitoids that coexist in spite of competition for resources. One potential mechanism for coexistence of competitors is a tradeoff between dispersiveness and local competitive ability. Here we present a study of competition between the specialized parasitoids Hyposoter horticola and Cotesia melitaearum sharing the Glanville fritillary butterfly, Melitaea cinxia . Within one host generation, the parasitoid larvae interact inside the host during each of the three C. melitaearum generations. We founds that in the summer when the host is small, the solitary H. horticola is the superior competitor, suppressing the gregarious C. melitaearum as eggs or small larvae. When multiparasitism occurs in the autumn the two parasitoid species engage in physical combat and C. melitaearum is favoured. Finally, a previous study showed that in the third C. melitaearum generation the univoltine H. horticola grows quickly during its final instar, excluding young C. melitaearum simply through limited time and resources. We found that contrary to expectations of the evolution of gregariousness, C. melitaearum , which lives in sibling groups, has biting mandibles in the first instar while the solitary H. horticola has suctorial mouthparts. Previous studies suggest that the two parasitoids co-exist because H. Horticola is dispersive and C. melitaearum is a strong local competitor. However, putting together the results of this experiment and out recent understanding of the adult wasp foraging behaviours and large scale population dynamics, we conclude that H. horticola is both a superior local competitor and more dispersive than C. melitaearum . Cotesia melitaearum has no impact on the population dynamics of H. horticola , persisting as a fugitive using a small fraction the larvae left unparasitized by H. horticola .     

Behaviour of a specialist parasitoid, Cotesia melitaearum: from individual behaviour to metapopulation processes

Abstract. 1. Foraging behaviour and movement within and among host patches of the specialist parasitoid wasp Cotesia melitaearum (Braconidae) attacking the larvae of Melitaea cinxia (Nymphalidae) were studied in the field and in the laboratory.
2. In the field, female wasps aggregated in large host groups in the autumn and caused positive spatial density-dependent parasitism in the field. Wasps stayed longer with groups of pre-diapause caterpillars than with post-diapause caterpillars, but attacked them less frequently.
3. In the laboratory, wasps attacked larger larvae more readily than smaller larvae. Also in the laboratory, wasps exposed to larvae outside their protective webs showed differences in the rates at which they attacked larvae fed different diets, implicating host plant-derived chemicals as proximate cues for foraging wasps.
4. Mark–recapture studies indicated that there was a low rate of successful movement of wasps among groups of young larvae within a habitat patch in the autumn and no successful movement of wasps across non-habitat. In contrast, wasps moved frequently among groups of late-instar caterpillars in the spring.
5. Host caterpillars of different ages responded very differently to wasp attacks. Pre-diapause larvae remained in groups and used collective head-jerking behaviour to defend themselves, whereas post-diapause larvae dispersed away from the group immediately after being attacked.
6. Population and metapopulation level dynamics of the host–parasitoid interaction are discussed in light of these observations of the behaviour of individual wasps.     

Effects of Intraspecific Competition and Host-Parasitoid Developmental Timing on Foraging Behaviour of a Parasitoid Wasp

In a context where hosts are distributed in patches and susceptible to parasitism for a limited time, female parasitoids foraging for hosts might experience intraspecific competition. We investigated the effects of host and parasitoid developmental stage and intraspecific competition among foraging females on host-searching behaviour in the parasitoid wasp Hyposoter horticola. We found that H. horticola females have a pre-reproductive adult stage during which their eggs are not mature yet and they forage very little for hosts. The wasps foraged for hosts more once they were mature. Behavioural experiments showed that wasps’ foraging activity also increased as host eggs aged and became susceptible to parasitism, and as competition among foraging wasps increased.     

Intrinsic, inter-specific competition between egg, egg–larval, and larval parasitoids of plusiine loopers

Abstract.  1. Intrinsic, inter-specific competition between parasitoid wasp species is a key factor in ecological community dynamics and is particularly important for application in biological control. Here three parasitoid wasp species with overlapping host ranges and differing life history strategies were chosen to examine parasitoid–parasitoid interactions: the egg parasitoid Trichogramma pretiosum, the egg–larval, polyembryonic parasitoid wasp Copidosoma floridanum, and the gregarious larval parasitoid Glyptapanteles pallipes , with the plusiine loopers Acanthoplusia agnata and Trichoplusia ni as hosts.
2.  Copidosoma floridanum has been shown to be an intrinsically superior competitor against larval parasitoids because of their production and increased investment in a soldier larval caste during development, but little is known of their interactions with egg parasitoid species. Trichogramma pretiosum completely dominated intrinsic competition with C. floridanum regardless of oviposition order or sex of the C. floridanum egg.
3. Competition between C. floridanum and G. pallipes , however, depended on the host stage at which parasitism occurred, the sex of the C. floridanum egg, and parasitoid development time. Copidosoma floridanum outcompeted G. pallipes overall, despite the fact that G. pallipes injects a polyDNA virus into the host.
4. The sex of the C. floridanum egg was a significant factor in its ability to shift caste ratios to produce more soldiers in response to G. pallipes competition.
5. Only developing female C. floridanum responded to competition with G. pallipes by increasing the ratio of soldier to reproductive larvae, and this happened only when multiparasitism occurred in the host's 1st and 2nd instar.     

Optimum and maximum host sizes at parasitism for the endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) differ greatly between two host species

Host size is considered a reliable indicator of host quality and an important determinant of parasitoid fitness. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism. In contrast with hemolymph-feeding koinobionts, tissue-feeding koinobionts face not only a minimum host size for successful development but also a maximum host size, because consumption of the entire host is often necessary for successful egression. Here we study interactions between a generalist tissue-feeding larval endoparasitoid, Hyposoter didymator Thunberg (Hymenoptera: Ichneumonidae) and two of its natural hosts, Spodoptera exigua Hübner and Chrysodeixis chalcites Esper (Lepidoptera: Noctuidae). Larvae of C. chalcites are up to three times larger than corresponding instars of S. exigua and also attain much higher terminal masses before pupation. We hypothesized that the range of host instars suitable for successful parasitism by H. didymator would be much more restricted in the large host C. chalcites than in the smaller S. exigua. To test this hypothesis, we monitored development of H. didymator in all instars of both host species and measured survival, larval development time, and adult body mass of the parasitioid. In contrast with our predictions, C. chalcites was qualitatively superior to S. exigua in terms of the survival of parasitized hosts, the proportion of parasitoids able to complete development, and adult parasitoid size. However, in both hosts, the proportion of mature parasitoid larvae that successfully developed into adults was low at the largest host sizes. Our results suggest that qualitative, as well as quantitative, factors are important in the success of tissue-feeding parasitoids.     

Metapopulation genetic structure of two coexisting parasitoids of the Glanville fritillary butterfly

We investigated the metapopulation genetic structure of two specialist parasitoids, Cotesia melitaearum and Hyposoter horticola, attacking the Glanville fritillary butterfly (Melitaea cinxia) in the Åland Islands south-western Finland. The host butterfly persists as a classic metapopulation in a network of 4,000 small habitat patches within an area of 50 by 70 km . The two parasitoids are known to differ greatly in their population dynamics and spatial pattern of occupancy in local host populations. Analysis of genetic population structure using F_ST and clustering of multilocus genotypes revealed a distinct large-scale spatial structure in C. melitaearum but a very weak pattern in H. horticola. This result is consistent with the known difference in the dispersal range (much longer in H. horticola) and population size (much greater in H. horticola) of the two parasitoids.     

Competition and coexistence in regional habitats

Habitat heterogeneity plays a key role in the dynamics and structures of communities. In this article, a two-species metapopulation model that includes local competitive dynamics is analyzed to study the population dynamics of two competing species in spatially structured habitats. When local stochastic extinction can be ignored, there are, as in Lotka-Volterra equations, four outcomes of interspecific competition in this model. The outcomes of competition depend on the competitive intensity between the competing pairs. An inferior competitor and a superior competitor, or two strongly competing species, can never stably coexist, whereas two weak competitors (even if they are very similar species) may coexist over the long term in such environments. Local stochastic extinction may greatly affect the outcomes of interspecific competition. Two competing species can or cannot stably coexist depending not only on the competitive intensity between the competing pairs but also on their precompetitive distributions. Two weak competitors that have similar precompetitive distributions can always regionally coexist. Two strongly competing species that competitively exclude each other in more stable habitats may be able to stably coexist in highly heterogenous environments if they have similar precompetitive distributions. There is also a chance for an inferior competitor to coexist regionally or even to exclude a superior competitor when the superior competitor has a narrow precompetitive distribution and the inferior competitor has a wide precompetitive distribution.     

Parasites promote host gene flow in a metapopulation

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

Causes and consequences of small population size for a specialist parasitoid wasp

The parasitoid wasp Cotesia melitaearum lives in extremely small extinction-prone populations in the Åland islands of southwest Finland. Intensive observational data from two generations, a laboratory competition experiment, and 8 years of survey data were used to measure the causes, extent and consequences of small population size for this parasitoid. In the spring generations of 1999 and of 2000 we observed 21 out of 23 and 26 populations respectively, ranging in size from 2 to 103 parasitoid cocoons. Within these populations the fraction of individuals surviving to adulthood decreased with increasing parasitoid population size. The largest source of mortality was predation (44%) followed by parasitism (20%) and unknown causes (10%). In the field about 30% of the host butterfly larvae are parasitized by a competing parasitoid, Hyposoter horticola. A laboratory competition experiment showed that C. melitaearum eggs died when laid in post-diapause host larvae occupied by H. horticola. Consequently one-third of the progeny of the over-wintering generation of C. melitaearum from the field die as a result of larval competition. The survey of host and parasitoid population dynamics over 8 years showed that extinction of local host butterfly populations occupied by the parasitoid was not associated with current parasitoid population size. Over the same period small parasitoid populations were more likely to become extinct than large populations. However, parasitoid population size was not related to parasitoid extinction when the host also became extinct. These data suggest that the parasitoid populations are kept small through the action of natural enemies and competitors, some of which are density dependent. Local populations are so small that they become extinct frequently and rarely measurably affect the population dynamics of their host. It is likely that this parasitoid persists in Åland because of the spatial asynchrony of local population dynamics.     

Spatial ecology of host–parasitoid interactions: a threatened butterfly and its specialised parasitoid

Habitat conservation for threatened temperate insect species is often guided by one of two paradigms: a metapopulation approach focusing on patch area, isolation and number; or a habitat approach focusing on maintaining high quality habitat for the focal species. Recent research has identified the additive and interacting importance of both approaches for maintaining populations of threatened butterflies. For specialised host-parasitoid interactions, understanding the consequences of habitat characteristics for the interacting species is important, because (1) specialised parasitoids are particularly vulnerable to the consequences of fragmentation, and (2) altered interaction frequencies resulting from changes to habitat management or the spatial configuration of habitat are likely to have consequences for host dynamics. The spatial ecology of Cotesia bignellii, a specialist parasitoid of the threatened butterfly Euphydryas aurinia, was investigated at two spatial scales: within habitat patches (at the scale of individual aggregations of larvae, or ‘webs’) and among habitat patches (the scale of local populations). Parasitism rates were investigated in relation to larval web size, vegetation sward height and host density. Within patches, the probability of a larval webs being parasitized increased significantly with increasing number of larvae in the web, and parasitism rates increased significantly with increasing web isolation. The proportion of webs parasitized was significantly and negatively correlated with cluster density. Among habitat patches the proportion of parasitized webs decreased as cluster density increased. Clusters with a high proportion of larval webs parasitized tended to have lower parasitism rates per larval web. These results support the call for relatively large and continuous habitat patches to maintain stable parasitoid and host populations. Conservation efforts directed towards maintenance of high host plant density could allow E. aurinia to reduce parasitism risk, while providing C. bignellii with sufficient larval webs to allow population persistence.     

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

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

Population size dependence, competitive coexistence and habitat destruction

1. Spatial dynamics can lead to coexistence of competing species even with strong asymmetric competition under the assumption that the inferior competitor is a better colonizer given equal rates of extinction. Patterns of habitat fragmentation may alter competitive coexistence under this assumption.
2. Numerical models were developed to test for the previously ignored effect of population size on competitive exclusion and on extinction rates for coexistence of competing species. These models neglect spatial arrangement.
3. Cellular automata were developed to test the effect of population size on competitive coexistence of two species, given that the inferior competitor is a better colonizer. The cellular automata in the present study were stochastic in that they were based upon colonization and extinction probabilities rather than deterministic rules.
4. The effect of population size on competitive exclusion at the local scale was found to have little consequence for the coexistence of competitors at the metapopulation (or landscape) scale. In contrast, population size effects on extinction at the local scale led to much reduced landscape scale coexistence compared to simulations not including localized population size effects on extinction, especially in the cellular automata models. Spatially explicit dynamics of the cellular automata vs. deterministic rates of the numerical model resulted in decreased survival of both species. One important finding is that superior competitors that are widespread can become extinct before less common inferior competitors because of limited colonization.
5. These results suggest that population size–extinction relationships may play a large role in competitive coexistence. These results and differences are used in a model structure to help reconcile previous spatially explicit studies which provided apparently different results concerning coexistence of competing species.     

The influence of two endoparasitic wasps, <Emphasis Type="Italic">Hyposoter didymator</Emphasis> and <Emphasis Type="Italic">Chelonus inanitus</Emphasis>, on the growth and food consumption of their host larva <Emphasis Type="Italic">Spodoptera littoralis</Emphasis>

The influence of parasitism by Hyposoter didymator (Thunberg; Hymenoptera: Ichneumonidae) and Chelonus inanitus (Linnaeus) (Hymenoptera: Braconidae) on the growth and food consumption of their host Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) was studied in the laboratory. Parasitised larvae consumed significantly less artificial diet than unparasitised ones. Egg parasitisation by C. inanitus affected host larval consumption from the second day after emergence and it was significantly different from that of unparasitised ones. H. didymator, however, started to reduce larval consumption 4 days after parasitisation on the third instar host larvae. The overall reduction achieved by the larval endoparasitoid H. didymator is higher than that caused by the egg-larval endoparasitoid C. inanitus. The final body weight of a parasitised host larva by H. didymator and C. inanitus was only 6.7 and 13.0% of the maximum weight of an unparasitised sixth instar larva respectively. Moreover, parasitised larvae never reached the last instar. Results indicated that parasitised larvae might cause considerable less damage to the host plant than unparasitised ones.     

Host-specific variation in Ieaf miner population dynamics: effects on density, natural enemies and behaviour of Stilbosis quadricustatella (Lepidoptera: Cosmopterigidae)

Abstract. 1. We compared high and low density populations of a leaf miner ( Stilbosis quadricustatella (Cham.)) on two host oaks to ascertain mechanisms influencing abundance. High density miner populations occurred on sand live oak, Quercus geminata (Fagaceae), found in homogeneous stands at inland and coastal sites. Quercus nigra , water oak, a patchily distributed inland species, supported a low density leaf miner population.
2. Average foliar nitrogen of Q.geminata was significantly lower than that of Q.nigra , and lad mining period on Q.geminata was correspondingly longer than on Q.nigra .
3. The average leaf area of Q.nigra was significantly greater than that of Q.geminata .
4. Parasitism was significantly greater in Q.geminata miner populations and predation was significantly higher in Q.nigra populations. However, parasitism and predation rates were roughly reciprocal so that overall larval mortality did not differ significantly between hosts.
5. In a laboratory experiment, pupal overwintering survivorship did not differ significantly between moist and dry treatments of the sand and loam soil types that typify Qgeminata and Q.nipra habitats, respectively.
6. Within-leaf miner density on Q.geminata significantly affected larval survivorship, parasitism and predation. Leaf area and within-leaf miner density were positively correlated.
7. We detected no host-patch area or isolation effect on miner densities on coastal Qgeminata and there was no significant gradient of local coastal conditions affecting larval survivorship or natural enemies.
8. Coastal leaf miner densities were significantly higher on oak patch edges than in interiors.     

Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species

Patch occupancy theory predicts that a trade-off between competition and dispersal should lead to regional coexistence of competing species. Empirical investigations, however, find local coexistence of superior and inferior competitors, an outcome that cannot be explained within the patch occupancy framework because of the decoupling of local and spatial dynamics. We develop two-patch metapopulation models that explicitly consider the interaction between competition and dispersal. We show that a dispersal-competition trade-off can lead to local coexistence provided the inferior competitor is superior at colonizing empty patches as well as immigrating among occupied patches. Immigration from patches that the superior competitor cannot colonize rescues the inferior competitor from extinction in patches that both species colonize. Too much immigration, however, can be detrimental to coexistence. When competitive asymmetry between species is high, local coexistence is possible only if the dispersal rate of the inferior competitor occurs below a critical threshold. If competing species have comparable colonization abilities and the environment is otherwise spatially homogeneous, a superior ability to immigrate among occupied patches cannot prevent exclusion of the inferior competitor. If, however, biotic or abiotic factors create spatial heterogeneity in competitive rankings across the landscape, local coexistence can occur even in the absence of a dispersal-competition trade-off. In fact, coexistence requires that the dispersal rate of the overall inferior competitor not exceed a critical threshold. Explicit consideration of how dispersal modifies local competitive interactions shifts the focus from the patch occupancy approach with its emphasis on extinction-colonization dynamics to the realm of source-sink dynamics. The key to coexistence in this framework is spatial variance in fitness. Unlike in the patch occupancy framework, high rates of dispersal can undermine coexistence, and hence diversity, by reducing spatial variance in fitness.     

Host relations, life cycles and multiparasitism in some parasitoids of aphidophagous Syrphidae (Diptera)

Abstract. 1. Records of parasitism from the field and host choice experiments suggest that most parasitoids of syrphids are monophagous. A few are oligophagous.
2. To elicit egg release, females require a stimulus from the host haemolymph. Differential response to haemolymph cues by females may account for the observed pattern of host relations.
3. Differences in host ranges and timing of female flight periods probably characterize most of the parasitoids studied.
4. In one case of two monophagous parasitoids, Diplazon pectoratorius (Thunberg) and Syrphophilus tricinctorius (Thunberg) attacking the same host Syrphus ribesii (L.) no partitioning was found. Stricinctorius is, however, a superior intrinsic competitor.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

Apparent competition between parasitoids mediated by a shared hyperparasitoid

Cocoons of the specialist parasitoid Cotesia melitaearum , which attacks the Glanville fritillary butterfly in the Åland islands of SW Finland, are parasitized by the generalist hyperparasitoid Gelis agilis . We added experimentally to the system a second host species for G. agilis , C. glomerata , with which C. melitaearum does not compete for resources. After the one-time addition of the second parasitoid the natural populations of C. melitaearum declined in the treatment, as predicted by the apparent competition theory.     

A parasitoid wasp uses landmarks while monitoring potential resources

Social insects and insects that provision nests are well known to have complex foraging behaviour involving repeated visits to learned locations. Other insects do not forage from a central location and are generally assumed to respond to resources by simple attraction without spatial memory. This simple response to resource cues is generally taken as giving rise to patterns of resource use that correspond directly to resource distribution. By contrast, the solitary parasitoid wasp Hyposoter horticola monitors the locations of multiple potential hosts (butterfly eggs) for up to several weeks, until the hosts become susceptible to parasitism. Essentially all hosts in the landscape are found, and one-third of them are parasitized, independent of host density. Here, we show that the wasps do not relocate hosts using odour markers previously left by themselves or other foragers, nor do they find the eggs anew repeatedly. Instead, the wasps relocate host eggs by learning the position of the eggs relative to visual landmarks. The anticipatory foraging behaviour presented here is a key to the wasp's exceptionally stable population dynamics.     

The importance of specialist natural enemies for Chrysomela lapponica in pioneering a new host plant

Abstract.  1. The Salicaceae have been suggested as ancestral host plants of Chrysomela species (Coleoptera: Chrysomelidae). In Chrysomela lapponica , some populations are specialised on salicaceous plants, but others have switched to birch. This study aimed to elucidate the significance of natural enemies as possible selective forces for the host plant shift of C. lapponica from willow to birch.
2. Two C. lapponica populations were studied, one specialised on willow Salix borealis in Finland, and another one specialised on birch Betula pubescens in the Czech Republic. Abundances of predators and parasitoids on birches and willows were recorded at both population sites. Furthermore, field and laboratory experiments were conducted.
3. Field data do not support the hypothesis that generalist predators affected the host shift from willow to birch in C. lapponica.
4. Parasitism of C. lapponica (pre)pupae by a specialised phorid fly was significantly stronger in specimens living on willow than in birch-living ones.
5. The predatory syrphid Parasyrphus nigritarsis specialised on Chrysomelinae was only detected on willows. The syrphid preferred to orient towards substrates treated with defensive larval secretion or faeces of the willow-specialised C. lapponica specimens compared with the birch-specialised ones.
6. The data suggest that specialised parasitoids and predators might have been driving forces for C. lapponica to leave willows and to pioneer birches as sites with a lowered risk of predation and parasitism. This hypothesis is discussed with respect to results of earlier studies on the impact of bottom-up effects by the plant.