Michal Segoli

Ecoinformatics for Integrated Pest Management: Expanding the Applied Insect Ecologist's Tool-Kit

ABSTRACT Experimentation has been the cornerstone of much of integrated pest management (IPM) research. Here, we aim to open a discussion on the possible merits of expanding the use of observational studies, and in particular the use of data from farmers or private pest management consultants in “ecoinformatics” studies, as tools that might complement traditional, experimental research. The manifold advantages of experimentation are widely appreciated: experiments provide definitive inferences regarding causal relationships between key variables, can produce uniform and high-quality data sets, and are highly flexible in the treatments that can be evaluated. Perhaps less widely considered, however, are the possible disadvantages of experimental research. Using the yield-impact study to focus the discussion, we address some reasons why observational or ecoinformatics approaches might be attractive as complements to experimentation. A survey of the literature suggests that many contemporary yield-impact studies lack sufficient statistical power to resolve the small, but economically important, effects on crop yield that shape pest management decision-making by farmers. Ecoinformatics-based data sets can be substantially larger than experimental data sets and therefore hold out the promise of enhanced power. Ecoinformatics approaches also address problems at the spatial and temporal scales at which farming is conducted, can achieve higher levels of “external validity,” and can allow researchers to efficiently screen many variables during the initial, exploratory phases of research projects. Experimental, observational, and ecoinformatics-based approaches may, if used together, provide more efficient solutions to problems in pest management than can any single approach, used in isolation.

Developmental patterns in the polyembryonic parasitoid wasp Copidosoma koehleri.

Polyembryony is a unique mode of development in which multiple genetically identical embryos develop from a single egg. In some polyembryonic species a proportion of the embryos develop into soldier larvae, which attack competitors in the host. We studied the development of the polyembryonic wasp Copidosoma koehleri in its host Phthorimaea opercullela. We dissected hosts parasitized by either virgin or mated female wasps at 2day intervals from hatching to the final instars. We documented host mass and head width, the number and size of developing wasps and the presence of a soldier larva. Additionally, we kept a sample of parasitized hosts until emergence of wasps and measured the head width of emerging adults. We characterized wasp development in relation to host development. One half of the broods produced by mated wasps contained one soldier larva throughout development. This suggests that in C. koehleri each female brood produces a single soldier larva, and that the soldier probably survives and grows gradually during host development. Additionally, we found that female broods were larger than male broods during development and also upon emergence. Accordingly, body size was larger for males during development as well as upon emergence. These findings may extend the existing knowledge on polyembryonic development in general, and serve as a baseline for further experiments.

The link between host density and egg production in a parasitoid insect: comparison between agricultural and natural habitats

Summary Theory predicts that organisms should invest more heavily in overcoming factors that more frequently emerge as the primary constraints to fitness, and especially, those factors that constrain the fitness of the most highly reproductive members of the population. We tested the hypothesis that the fecundity of a pro-ovigenic parasitoid (where females emerge with their full egg load) should be positively correlated with the mean expectation for oviposition opportunities in the environment. More specifically, we tested whether females from agricultural systems, where hosts are often relatively abundant, emerge with more eggs than those from natural habitats. We studied the pro-ovigenic parasitoid wasp Anagrus daanei, which parasitizes eggs of leafhoppers of the genus Erythroneura. Erythroneura spp. leafhoppers feed on Vitis spp. (grapes) and are major pests of commercial vineyards as well as common herbivores of wild Vitis californica, which grows in riparian habitats. We sampled leafhoppers and parasitoids from eight vineyards and eight riparian habitats in central California. We found that leafhopper density was higher at vineyards than in riparian habitats, whereas leafhopper egg volume and parasitoid body size did not differ among these habitat types. Parasitoids from vineyards had higher egg loads than parasitoids from wild grapes, and fecundity was positively related to host density across field sites. Parasitoid egg volume was larger in natural sites; however, this variation was not significantly correlated with host density across field sites. Within a single population of parasitoids collected from a vineyard, parasitoid egg load was negatively correlated with longevity, suggesting a trade-off between reproduction and life span. The results may be explained by a rapid evolution of reproductive traits in response to oviposition opportunities; or alternatively, by the occurrence of maternal effects on the fecundity of daughters based on the foraging experience of their mothers. The ability of parasitoid fecundity to track mean host availability is likely to modulate the likelihood that parasitoid fitness will be constrained by a shortage of eggs and strengthen the ability of parasitoids to suppress the population densities of their hosts.

Limits to the reproductive success of two insect parasitoid species in the field.

Debates on the relative importance of different factors in limiting the realized fitness of insect parasitoids and herbivores have continued for decades. One major reason for the duration of these debates is the paucity of empirical evidence regarding the reproductive success of minute insects under field conditions. We used a novel technique to estimate lifetime reproductive success in two Anagrus spp. parasitoids, whose hosts are eggs of leafhoppers that feed on grape leaves. Females were collected soon after they died naturally, and the number of eggs in their ovaries was counted. We used these data to estimate the lifetime oviposition success of individual females. We found that more than 10% of females from the field exhausted their entire supply of eggs before they died. The lifetime reproductive success of females was positively related to their body size and was higher at field sites with more abundant hosts, although we could not rule out a causal role for other site-specific factors. In addition, we found that females from habitats rich with hosts emerged with more eggs, suggesting that they might be adapted to local conditions. The results are consistent with theoretical predictions from models considering the risk of egg limitation.

Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae)

Female parasitoids often reject hosts of poor quality, where the survival and fitness of their offspring are expected to be low. In polyembryonic parasitoid wasps, a clone of genetically identical embryos develops from one egg in a host. In the wasp Copidosoma koehleri, each female clone produces one soldier larva that attacks competing clones inside the host. Aggression by soldiers is directed usually towards unrelated clones. Accordingly, it may be predicted that females will prefer nonparasitized over parasitized hosts, especially if the latter have been parasitized previously by a mated unrelated female, as a result of the reduced chances of survival for their offspring inside these hosts. In accordance with these predictions, females prefer nonparasitized hosts over self‐parasitized hosts when they are presented simultaneously. By contrast to the predictions, females prefer hosts parasitized by an unrelated conspecific over nonparasitized hosts when presented simultaneously. Females do not distinguish hosts parasitized by conspecifics from self‐parasitized hosts when presented simultaneously. They reject self‐parasitized hosts significantly more often than hosts parasitized by conspecifics when each host type is presented alone. Females faced with two previously parasitized hosts are not affected in their choice by the mating status (i.e. virgin or mated) of the previous parasitizing females. The combined results suggest that females are limited in their ability to assess the risk that their offspring will be attacked by a soldier, or that this risk is balanced by the relative advantages of ovipositing in a host parasitized by conspecifics. A possible advantage may be increased out‐breeding opportunities for the emerging offspring.

Frequency and consequences of damage to male copulatory organs in a widow spider

Abstract Copulatory organ breakage, in which a portion of the males genitalia breaks off and remains in or attached to the females genitalia may represent a male strategy of high investment in a single mating. Such a strategy is expected when mating opportunities for males are limited and competition for females is high. We studied costs and benefits for males as a consequence of male organ breakage in the white widow spider (Latrodectus pallidus O. Pickard-Cambridge 1872). In order to estimate the frequency and consequences of such damage we provided each male with four virgin females simultaneously in an outdoors enclosure. We recorded male mating success and loss of the tip of the embolus (the male intromittent organ) inside the females genitalia for each male. In order to test the effect of the broken tip as a mating plug, we collected females from natural populations and observed the location of embolus tips inside their genitalia. We found that damage to the male organ was frequent but did not necessarily result in male sterility. From the field data, we found that the likelihood of a second embolus tip entering the spermatheca is significantly lower than that of the first tip, suggesting the possibility that the tip functions as a partial mating plug.

The effect of body size on oviposition success of a minute parasitoid in nature

1. Individual fitness is often assumed to be positively correlated with body size, but this has rarely been explored under realistic field conditions. This assumption was tested in a minute parasitoid foraging for planthopper eggs in saltmarsh habitats.

The mating status of mothers and offspring sex affect clutch size in a polyembryonic parasitoid wasp

Mothers can modify the phenotype of their offspring both genetically and epigenetically, in response to the environment they experience. The role of maternal experience in affecting offspring clutch size is often difficult to measure, because parent–offspring conflict over this trait is common. In polyembryonic parasitoids, where each egg proliferates to form a clone of genetically identical siblings, the conflict is minimized. Therefore, they are good models for studying maternal effects on clutch size. In the haplodiploid parasitoid wasp Copidosoma koehleri, female clones contain more individuals than male clones. This may result from differences in genome size or in optimal body size between the sexes. Alternatively, maternal mating may mediate epigenetic physiological changes in eggs, leading to increased proliferation. We evaluated these hypotheses by comparing the body size and number of clone mates produced by mated versus virgin females. Sons of mated females were significantly smaller and formed larger clones than sons of virgins. Daughters formed the largest clones, but resembled sons of mated females in body size. Clone sizes of parents and offspring were not correlated. These findings suggest that both offspring sex and maternal experience (mating status) affect clone size, and that this trait’s heritability is low. The increased proliferation by offspring of mated females may enhance paternal fitness by producing extra daughters, or benefit the offspring under conditions where the associated decrease in body size does not greatly reduce fitness. We estimated the contribution of large body size to male reproductive success through a mate choice assay.

Host Handling Time in a Polyembryonic Wasp is Affected both by Previous Experience and by Host State (Parasitized or Not)

Foraging behavior for hosts in parasitoids resembles that of predators with respect to finding, evaluating and manipulating of the prey. Host handling time may depend on the life history of the parasitoid and can be affected by oviposition experience. Additionally, handling time can be affected by host aggregation, species, size and state (parasitized or not). We studied handling times in the egg-larval parasitoid wasp Copidosoma koehleri. We allowed naïve female wasps to oviposit into three consecutive unparasitized hosts, and measured time until oviposition, and the duration of ovipositor insertion. We recorded the same data for naïve females ovipositing into already parasitized hosts. We found that both previous experience by females and previous parasitism of hosts reduced handling time. The results suggest that host handling durations reflect the interplay between host state and parasitoid internal state.

Factors shaping life history traits of two proovigenic parasitoids

What shapes the relative investment in reproduction versus survival of organisms is among the key questions in life history. Proovigenic insects mature all their eggs prior to emergence and are short lived, providing a unique opportunity to quantify their lifetime investments in the different functions. We investigated the initial eggloads and longevity of 2 proovigenic parasitoid wasps: Anagrus erythroneurae and Anagrus daanei, (Hymenoptera: Mymaridae) that develop within leafhopper eggs in both agricultural vineyards and natural riparian habitats in Northern California. We collected Vitis spp. leaves containing developing parasitoids from 3 natural sites (Knight Landing, American River and Putah Creek) and 3 agricultural vineyards (Solano Farm, Davis Campus and Village Homes). We recorded eggloads at parasitoid emergence and female parasitoid longevity with or without honey-feeding. Theory predicts that parasitoids from vineyards (where hosts are abundant) would have higher initial eggloads and lower longevity compared with parasitoids from riparian habitats (where hosts are scarce). Although host density and parasitoid eggloads were, indeed, higher in vineyards than in riparian habitats, parasitoid longevity did not follow the predicted pattern. Longevity without feeding differed among field sites, but it was not affected by habitat type (natural vs agricultural), whereas longevity with feeding was not significantly affected by any of the examined factors. Moreover, longevity was positively, rather than negatively, correlated with eggloads at the individual level, even after correcting for parasitoid body size. The combined results suggest a more complex allocation mechanism than initially predicted, and the possibility of variation in host quality that is independent of size.