Dynamic Economic Thresholds for Insecticide Applications Against Agricultural Pests: Importance of Pest and Natural Enemy Migration.

In Integrated Pest Management programs, insecticides are applied to agricultural crops when pest densities exceed a predetermined economic threshold. Under conditions of high natural enemy density, however, the economic threshold can be increased, allowing for fewer insecticide applications. These adjustments, called 'dynamic thresholds', allow farmers to exploit existing biological control interactions without economic loss. Further, the ability of natural enemies to disperse from, and subsequently immigrate into, insecticide-sprayed areas can affect their biological control potential. We develop a theoretical approach to incorporate both pest and natural enemy movement across field borders into dynamic thresholds and explore how these affect insecticide applications and farmer incomes. Our model follows a pest and its specialist natural enemy over one growing season. An insecticide that targets the pest also induces mortality of the natural enemy, both via direct toxicity and reduced resource pest densities. Pest and natural enemy populations recover after spraying through within-field reproduction and by immigration from neighboring unsprayed areas. The number of insecticide applications and per-season farmer revenues are calculated for economic thresholds that are either fixed (ignoring natural enemy densities) or dynamic (incorporating them). The model predicts that using dynamic thresholds always leads to reduced insecticide application. The benefit of dynamic thresholds in reducing insecticide use is highest when natural enemies rapidly recolonize sprayed areas, and when insecticide efficacy is low. We discuss real-life situations in which monitoring of natural enemies would substantially reduce insecticide use and other scenarios where the presence of beneficial organisms may lead to threshold modifications.

Metapopulation capacity determines food chain length in fragmented landscapes.

Metapopulation capacity provides an analytic tool to quantify the impact of landscape configuration on metapopulation persistence, which has proven powerful in biological conservation. Yet surprisingly few efforts have been made to apply this approach to multispecies systems. Here, we extend metapopulation capacity theory to predict the persistence of trophically interacting species. Our results demonstrate that metapopulation capacity could be used to predict the persistence of trophic systems such as prey-predator pairs and food chains in fragmented landscapes. In particular, we derive explicit predictions for food chain length as a function of metapopulation capacity, top-down control, and population dynamical parameters. Under certain assumptions, we show that the fraction of empty patches for the basal species provides a useful indicator to predict the length of food chains that a fragmented landscape can support and confirm this prediction for a host-parasitoid interaction. We further show that the impact of habitat changes on biodiversity can be predicted from changes in metapopulation capacity or approximately by changes in the fraction of empty patches. Our study provides an important step toward a spatially explicit theory of trophic metacommunities and a useful tool for predicting their responses to habitat changes.

Long-term spatiotemporal genetic structure of an accidental parasitoid introduction, and local changes in prevalence of its associated Wolbachia symbiont.

Population bottlenecks associated with founder events strongly impact the establishment and genetic makeup of populations. In addition to their genotype, founding individuals also bring along parasites, as well as symbionts that can manipulate the phenotype of their host, affecting the host population establishment, dynamics and evolution. Thus, to understand introduction, invasion, and spread, we should identify the roles played by accompanying symbionts. In 1991, the parasitoid wasp, Hyposoter horticola, and its associated hyperparasitoid were accidentally introduced from the main Åland islands, Finland, to an isolated island in the archipelago, along with their host, the Glanville fritillary butterfly. Though the receiving island was unoccupied, the butterfly was present on some of the small islands in the vicinity. The three introduced species have persisted locally ever since. A strain of the endosymbiotic bacterium Wolbachia has an intermediate prevalence in the parasitoid H. horticola across the main Åland population. The infection increases its susceptibility of to hyperparasitism. We investigated the establishment and spread of the parasitoid, along with patterns of prevalence of its symbiont using 323 specimens collected between 1992 and 2013, from five localities across Åland, including the source and introduced populations. Using 14 microsatellites and one mitochondrial marker, we suggest that the relatively diverse founding population and occasional migration between islands might have facilitated the persistence of all isolated populations, despite multiple local population crashes. We also show that where the hyperparasitoid is absent, and thus selection against infected wasp genotypes is relaxed, there is near-fixation of Wolbachia.

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

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

Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid.

Climate change can increase spatial synchrony of population dynamics, leading to large-scale fluctuation that destabilizes communities. High trophic level species such as parasitoids are disproportionally affected because they depend on unstable resources. Most parasitoid wasps have complementary sex determination, producing sterile males when inbred, which can theoretically lead to population extinction via the diploid male vortex (DMV). We examined this process empirically using a hyperparasitoid population inhabiting a spatially structured host population in a large fragmented landscape. Over four years of high host butterfly metapopulation fluctuation, diploid male production by the wasp increased, and effective population size declined precipitously. Our multitrophic spatially structured model shows that host population fluctuation can cause local extinctions of the hyperparasitoid because of the DMV. However, regionally it persists because spatial structure allows for efficient local genetic rescue via balancing selection for rare alleles carried by immigrants. This is, to our knowledge, the first empirically based study of the possibility of the DMV in a natural host-parasitoid system.

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.

Higher predation risk for insect prey at low latitudes and elevations.

Biotic interactions underlie ecosystem structure and function, but predicting interaction outcomes is difficult. We tested the hypothesis that biotic interaction strength increases toward the equator, using a global experiment with model caterpillars to measure predation risk. Across an 11,660-kilometer latitudinal gradient spanning six continents, we found increasing predation toward the equator, with a parallel pattern of increasing predation toward lower elevations. Patterns across both latitude and elevation were driven by arthropod predators, with no systematic trend in attack rates by birds or mammals. These matching gradients at global and regional scales suggest consistent drivers of biotic interaction strength, a finding that needs to be integrated into general theories of herbivory, community organization, and life-history evolution.

The more the merrier: Conspecific density improves performance of gregarious larvae and reduces susceptibility to a pupal parasitoid.

Aggregation can confer advantages in animal foraging, defense, and thermoregulation. There is a tight connection between the evolution of insect sociality and a highly effective immune system, presumably to inhibit rapid disease spread in a crowded environment. This connection is less evident for animals that spend only part of their life cycle in a social environment, such as noneusocial gregarious insects. Our aim was to elucidate the effects of group living by the gregarious larvae of the Glanville fritillary butterfly with respect to individual performance, immunity, and susceptibility to a parasitoid. We were also interested in the role of family relative to common postdiapause environment in shaping life-history traits. Larvae were reared at high or low density and then exposed to the pupal parasitoid wasp Pteromalus apum, either in presence or absence of a previous immune challenge that was used to measure the encapsulation immune response. Surviving adult butterflies were further tested for immunity. The wasp offspring from successfully parasitized butterfly pupae were counted and their brood sex ratios assessed. Larvae reared at high density grew larger and faster than those at low density. Despite high mortality due to parasitism, survival was greater among individuals with high pupal immunity in both density treatments. Moreover, butterfly pupae reared at high density were able to kill a larger fraction of individuals in the parasitoid broods, although this did not increase survival of the host. Finally, a larger proportion of variation observed in most of the traits was explained by butterfly family than by common postdiapause rearing environment, except for adult survival and immunity, for which this pattern was reversed. This gregarious butterfly clearly benefits from high conspecific density in terms of developmental performance and its ability to fight a parasitoid. These positive effects may be driven by cooperative interactions during feeding.

Wolbachia increases the susceptibility of a parasitoid wasp to hyperparasitism.

The success of maternally transmitted endosymbiotic bacteria, such as Wolbachia, is directly linked to their host reproduction but in direct conflict with other parasites that kill the host before it reaches reproductive maturity. Therefore, symbionts that have evolved strategies to increase their host's ability to evade lethal parasites may have high penetrance, while detrimental symbionts would be selected against, leading to lower penetrance or extinction from the host population. In a natural population of the parasitoid wasp Hyposoter horticola in the Åland Islands (Finland), the Wolbachia strain wHho persists at an intermediate prevalence (∼50%). Additionally, there is a negative correlation between the prevalence of Wolbachia and a hyperparasitoid wasp, Mesochorus cf. stigmaticus, in the landscape. Using a manipulative field experiment, we addressed the persistence of Wolbachia at this intermediate level, and tested whether the observed negative correlation could be due to Wolbachia inducing either susceptibility or resistance to parasitism. We show that infection with Wolbachia does not influence the ability of the wasp to parasitize its butterfly host, Melitaea cinxia, but that hyperparasitism of the wasp increases in the presence of wHho. Consequently, the symbiont is detrimental, and in order to persist in the host population, must also have a positive effect on fitness that outweighs the costly burden of susceptibility to widespread parasitism.

Diversity, population structure, and individual behaviour of parasitoids as seen using molecular markers.

Parasitoids have long been models for host-parasite interactions, and are important in biological control. Neutral molecular markers have become increasingly accessible tools, revealing previously unknown parasitoid diversity. Thus, insect communities are now seen as more speciose. They have also been found to be more complex, based on trophic links detected using bits of parasitoid DNA in hosts, and host DNA in adult parasitoids. At the population level molecular markers are used to determine the influence of factors such as host dynamics on parasitoid population structure. Finally, at the individual level, they are used to identify movement of individuals. Overall molecular markers greatly increase the value of parasitoid samples collected, for both basic and applied research, at all levels of study.

Spatial and temporal genetic structure at the fourth trophic level in a fragmented landscape.

A fragmented habitat becomes increasingly fragmented for species at higher trophic levels, such as parasitoids. To persist, these species are expected to possess life-history traits, such as high dispersal, that facilitate their ability to use resources that become scarce in fragmented landscapes. If a specialized parasitoid disperses widely to take advantage of a sparse host, then the parasitoid population should have lower genetic structure than the host. We investigated the temporal and spatial genetic structure of a hyperparasitoid (fourth trophic level) in a fragmented landscape over 50 × 70 km, using microsatellite markers, and compared it with the known structures of its host parasitoid, and the butterfly host which lives as a classic metapopulation. We found that population genetic structure decreases with increasing trophic level. The hyperparasitoid has fewer genetic clusters (K = 4), than its host parasitoid (K = 15), which in turn is less structured than the host butterfly (K = 27). The genetic structure of the hyperparasitoid also shows temporal variation, with genetic differentiation increasing due to reduction of the population size, which reduces the effective population size. Overall, our study confirms the idea that specialized species must be dispersive to use a fragmented host resource, but that this adaptation has limits.

Fatal diseases and parasitoids: from competition to facilitation in a shared host.

Diverse parasite taxa share hosts both at the population level and within individual hosts, and their interactions, ranging from competitive exclusion to facilitation, can drive community structure and dynamics. Emergent pathogens have the potential to greatly alter community interactions. We found that an emergent fungal entomopathogen dominated pre-existing lethal parasites in populations of the forest defoliating gypsy moth,Lymantria dispar The parasite community was composed of the fungus and four parasitoid species that only develop successfully after they kill the host, and a virus that produces viable propagules before the host has died. A low-density site was sampled over 17 years and compared with 66 sites across a range of host densities, including outbreaks. The emergent fungal pathogen and competing parasitoids rarely co-infected host individuals because each taxa must kill its host. The virus was not present at low host densities, but successfully co-infected with all other parasite species. In fact, there was facilitation between the virus and one parasitoid species hosting a polydnavirus. This newly formed parasite community, altered by an emergent pathogen, is shaped both by parasite response to host density and relative abilities of parasites to co-inhabit the same host individuals.

Wolbachia Infection in a Natural Parasitoid Wasp Population.

The maternally transmitted bacterium Wolbachia pipientis is well known for spreading and persisting in insect populations through manipulation of the fitness of its host. Here, we identify three new Wolbachia pipientis strains, wHho, wHho2 and wHho3, infecting Hyposoter horticola, a specialist wasp parasitoid of the Glanville fritillary butterfly. The wHho strain (ST435) infects about 50% of the individuals in the Åland islands in Finland, with a different infection rate in the two mitochondrial (COI) haplotypes of the wasp. The vertical transmission rate of Wolbachia is imperfect, and lower in the haplotype with lower infection rate, suggesting a fitness trade-off. We found no association of the wHho infection with fecundity, longevity or dispersal ability of the parasitoid host. However, preliminary results convey spatial associations between Wolbachia infection, host mitochondrial haplotype and parasitism of H. horticola by its hyperparasitoid, Mesochorus cf. stigmaticus. We discuss the possibility that Wolbachia infection protects H. horticola against hyperparasitism.

The puzzle of partial resource use by a parasitoid wasp.

When there is conspicuous underexploitation of a limited resource, it is worth asking, what mechanisms allow presumably valuable resources to be left unused? Evolutionary biologists have generated a wide variety of hypotheses to explain this, ranging from interdemic group selection to selfishly prudent individual restraint. We consider a situation in which, despite high intraspecific competition, individuals leave most of a key resource unexploited. The parasitic wasp that does this finds virtually all host egg clusters in a landscape but parasitizes only about a third of the eggs in each and then leaves a deterrent mark around the cluster. We first test-and reject-a series of system-specific simple constraints that might limit full host exploitation, such as asynchronous maturation of host eggs. We then consider classical hypotheses for the evolution of restraint. Prudent predation and bet-hedging fail as explanations because the wasp lives as a large, well-mixed population. Additionally, we find no individual benefits to the parasitoid of developing in a sparsely parasitized host nest. However, an optimal foraging model, including empirically measured costs of superparasitism and hyperparasitism, can explain through individual selection both the consistently low rate of parasitism and deterrent marking.

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.

Variation in a Host-Parasitoid Interaction across Independent Populations.

Antagonistic relationships between parasitoids and their insect hosts involve multiple traits and are shaped by their ecological and evolutionary context. The parasitoid wasp Cotesia melitaearum and its host butterfly Melitaea cinxia occur in several locations around the Baltic sea, with differences in landscape structure, population sizes and the histories of the populations. We compared the virulence of the parasitoid and the susceptibility of the host from five populations in a reciprocal transplant-style experiment using the progeny of five independent host and parasitoid individuals from each population. The host populations showed significant differences in the rate of encapsulation and parasitoid development rate. The parasitoid populations differed in brood size, development rate, pupal size and adult longevity. Some trait differences depended on specific host-parasitoid combinations, but neither species performed systematically better or worse in experiments involving local versus non-local populations of the other species. Furthermore, individuals from host populations with the most recent common ancestry did not perform alike, and there was no negative effect due to a history of inbreeding in the parasitoid. The complex pattern of variation in the traits related to the vulnerability of the host and the ability of the parasitoid to exploit the host may reflect multiple functions of the traits that would hinder simple local adaptation.

Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata.

The ability to cope with plant defense chemicals differs between specialist and generalist species. In this study, we examined the effects of the concentration of the two main iridoid glycosides (IGs) in Plantago lanceolata, aucubin and catalpol, on the performance of a specialist and two generalist herbivores and their respective endoparasitoids. Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant. By contrast, the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations, respectively. This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized. Melitaea cinxia experienced less post-diapause larval and pupal mortality on its local Finnish P. lanceolata than on Dutch genotypes. This could not be explained by differences in IG profiles, suggesting that M. cinxia has adapted in response to attributes of its local host plants other than to IG chemistry. Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M. cinxia, a response that was concordant with that of its host. By contrast, the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts, S. exigua and C. chalcites. While their hosts developed slowly on high-IG genotypes, development time of H. didymator was unaffected. Cotesia marginiventris actually developed faster on hosts fed high-IG genotypes, although they then had short adult longevity. The faster development of C. marginiventris on hosts that ate high-IG genotypes is in line with the "immunocompromized host" hypothesis, emphasizing the potential negative effects of toxic allelochemicals on the host's immune response.

Olfactory attraction of the larval parasitoid, Hyposoter horticola, to plants infested with eggs of the host butterfly, Melitaea cinxia.

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

Population dynamics and sex ratio of a parasitoid altered by fungal-infected diet of host butterfly.

Variation of host quality affects population dynamics of parasitoids, even at the landscape scale. What causes host quality to vary and the subsequent mechanisms by which parasitoid population dynamics are affected can be complex. Here, we examine the indirect interaction of a plant pathogen with a parasitoid wasp. Under laboratory conditions, parasitoids from hosts fed fungus-infected plants weighed less than those from hosts fed uninfected plants, indicating that the fungus causes the hosts to be of poor quality. However, parasitoids reared from hosts fed fungal-infected diet also tended to be female, a characteristic associated with high host quality. The pathogen, herbivore and parasitoid persist regionally as metapopulations in a shared landscape in Aland, Finland. In an analysis of the metapopulation dynamics of the parasitoid over 6 years, the probability of colonization of a host population increased by more than twofold in patches occupied by the plant pathogen. While we cannot determine that the relationship is causal, a compelling explanation is that the plant pathogen facilitates the establishment by the parasitoid by increasing the fraction of female offspring. This is a novel mechanism of spatial multi-trophic level interactions.