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We present a model for the population dynamics of the invasive fruit fly Drosophila suzukii and its pupal parasitoid Trichopria drosophilae. Seasonality of the environment is captured through a system of delay differential equations with variable delays. The model is used to explore optimal timing for releasing parasitoids in biological control programs. According to the results, releasing parasitoids is most effective between late spring and early summer when the host population begins to increase. A single parasitoid release event can be more efficient than multiple releases over a prolonged period, but multiple releases are more robust to suboptimal timing choices. The findings can be useful for optimizing parasitoid release and should be transferable for similar systems. More generally, the model is an example for stage-structured resource-consumer dynamics in a varying environment.

Between 1998 and 2017, we conducted studies in wild blueberry, Vaccinium angustifolium Aiton (Ericales: Ericaceae), to elucidate the temporal dynamics of the blueberry maggot fly, Rhagoletis mendax Curran, and its parasitoid, Biosteres melleus (Gahan). A predictive model for the emergence of R. mendax was validated at two sites over 3 yr. A second predictive model for the major parasitoid, B. melleus, of R. mendax was constructed and suggests that the delay in emergence of the parasitoid relative to its host provides a period or ‘biological window’ of 9 d where insecticide sprays can be applied to manage R. mendax with a limited impact on the parasitoid. A 20-yr study on the parasitoid/host dynamics showed parasitism rates ranging from 0.5 to 28.2%. It appears that R. mendax populations in Maine wild blueberry are characterized by stable equilibrium dynamics, significantly affected by stochastic processes. There was a weak, but significant relationship between B. melleus density and R. mendax intrinsic rates of growth. Our data suggest that R. mendax population dynamics in wild blueberry is characterized by an unstable equilibrium tipping point of 7.9 maggots per liter of blueberries or an average of 10 flies per trap.

Many natural enemies do not immediately kill their host, and the lag this creates between attack and host death results in mixed populations of uninfected and infected hosts. Both competition and parasitism are known to be major structuring forces in ecological communities; however, surprisingly little is known about how the competitive nature of infected hosts could affect the survival and dynamics of remaining uninfected host populations. Using a laboratory system comprising the Indian meal moth, Plodia interpunctella, and a solitary koinobiont parasitoid, Venturia canescens, we address this question by conducting replicated competition experiments between the unparasitized and parasitized classes of host larvae. For varying proportions of parasitized host larvae and competitor densities, we consider the effects of competition within (intraclass) and between (interclass) unparasitized and parasitized larvae on the survival, development time, and size of adult moths and parasitoid wasps. The greatest effects were on survival: increased competitor densities reduced survival of both parasitized and unparasitized larvae. However, unparasitized larvae survival, but not parasitized larvae survival, was reduced by increasing interclass competition. To our knowledge, this is the first experimental demonstration of the competitive superiority of parasitized over unparasitized hosts for limiting resources. We discuss possible mechanisms for this phenomenon, why it may have evolved, and its possible influence on the stability of host—parasite dynamics.

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.

Models of host handling decisions and physiologically structured host-par- asitoid population dynamics make diverging assumptions, untested as of this writing, about the allocation rules of nutrients to survival and reproduction. Our aim is to develop a datarich multidimensional dynamical budget of nutrient acquisition and allocation in survival and reproduction in the host-feeding, synovigenic bruchid ectoparasitoid Eupelmus vuilletti (Hymenoptera: Eupelmidae) over the entire lifetime of the animal in order to address the above questions. We quantified sugar, glycogen, protein, and lipid reserves of single females at birth and death and their daily maintenance needs. We recorded each host-feeding and oviposition event over entire lifetimes and quantified the amounts acquired and invested in eggs using microcolorimetric techniques. We then built two nutrient budgets, with and without hosts, encompassing 20 measured biochemical parameters and tested their predictions using time of death. Carbohydrate reserves are burned at a high rate for maintenance and can be used to predict lifetime in absence of hosts. The model without hosts is adequate, but the one with hosts is not, as it predicts a continuous increase of proteins from the massive host-feeding intake, contrasting with the observed decline. A good prediction of time of death could be achieved in that model by assuming that the large amounts of ingested proteins and carbohydrates from host-feeding are used for maintenance, thereby enabling females to spare lipids for reproduction. We tested this assumption in a treatment with hosts and supplemental sugars, in which the maximal number of produced eggs is expected to be almost exclusively a function of lipids when other nutrients can be obtained to cover maintenance costs. Our results enable us to discriminate between competing hypotheses about nutrient allocation in models of parasitoid behavior and host-parasitoid population dynamics. They show that E. vuilletti is both a capital breeder for lipids and an income breeder for sugars, implying that this dichotomy is best superseded by a multidimensional and dynamical approach to nutrient acquisition and allocation.

1. We studied the metapopulation dynamics and persistence of an extinction-prone predator-prey interaction. We show that the dynamics of the system are influenced by both stochastic and deterministic processes. 2. Using host-parasitoid metapopulation data, we develop appropriate descriptors of the local within-patch population dynamics. In particular, we show that the local dynamics are well described by a Markov chain. We show that the local dynamics are determined predominately by demographic stochastic processes and that the deterministic signal is relatively weak. 3. To test the hypothesis that the persistence of predator-prey metapopulations is affected by habitat size, local population dynamics and different types of (demographic or environmental) stochasticity, we fit population models to the regional metapopulation time-series. Contrary to expectations this demographic noise is, however, undetectable at the regional scale and is masked by an environmental noise process. We show that by linking patches together, the predicted environmental noise is effectively decreased as metapopulation size increases. 4. Using a simple spatial stochastic model, we illustrate that the effects of demographic noise are masked rapidly at the regional scale due to the statistical effects of the central limit theorem. We discuss the implications of this for understanding the dynamics and persistence of metapopulations.

The forest insect pest Bupalus piniarius (pine looper moth) is a classic example of a natural population cycle. As is typical for populations that exhibit regular oscillations in density, there are several biological mechanisms that are hypothesized to be responsible for the cycles; but despite several decades of detailed study there has been no definite conclusion as to which mechanism is most important. We evaluated three hypotheses for which there was direct experimental evidence: (1) food quality (nutritional value of pine needles affected by defoliation); (2) parasitoids (trophic interactions with specialist parasitoids); and (3) maternal effects (maternal body size affects the performance of offspring). We reviewed the empirical evidence for each of these hypotheses and expressed each hypothesis in the form of a mechanistic dynamic model. We used a nonlinear forecasting approach to fit each model to three long-term population time series in Britain that exhibit some degree of regular cycling, and we used parametric bootstrap to evaluate the significance of differences between models in their goodness of fit to the data. The results differed among the three forests: at Culbin, the parasitoid and maternal effects models fit equally well; at Roseisle, the food quality and maternal effects models fit equally well; and at Tentsmuir, the parasitoid model fit best. However, the best-fit parasitism models required that the parasitism rate vary between nearly 0 and nearly 1 during a cycle, greatly exceeding the range of parasitism rates that have been observed in the field. In contrast, the required variation in the observable maternal quality variable (pupal mass) was within the range of empirical observations. Under mild constraints on the parasitism rate (though allowing a much wider range than has been measured in B. piniarius at any location), the fit of the parasitism model fell off dramatically. The maternal effects model then had uniformly strong support, outperforming the constrained parasitism model at all three sites and the food quality model at two; it performed slightly better than the food quality model at the remaining site. This represents the first system in which the maternal effects hypothesis for population cycles has been supported by both strong biological and dynamical evidence.

Many ecological time series describe population dynamics. Indirectly, these data also provide information about the vital rates (e.g., birth rates, mortality rates) underlying these dynamics, but extracting this information from the data can be difficult. Here, we present a method for estimating fluctuating vital rates from ecological time series by using a model to re-code information in observed dynamics into information about unobserved vital rates. This model construction differs from most current models by replacing strong assumptions about the functional relationships dictating population dynamics with more conservative assumptions about how vital rates change with time. Thus, this method is a tool for analyzing time-series data that avoids strong assumptions about the mechanisms driving population dynamics. Our work is motivated by studying the biological control of pea aphids in alfalfa in south-central Wisconsin. Pea aphid populations are consistently held below economic threshold, although the source of this regulation is unclear. Here, we analyze monitoring data to understand the role that a specialist parasitoid plays in aphid biocontrol. Our modeling methodology allows us to estimate the vital rates that determine aphid dynamics (in particular, parasitism) without making arbitrary assumptions about the relationship between parasitism and aphid or parasitoid density. We find that, while parasitism depresses aphid population growth rate substantially, declines in aphid population growth rates do not coincide with increases in parasitism. Therefore, parasitism cannot be responsible for the density-dependent regulation of aphid populations observed in the field.

The biocontrol of insect pests may pose a risk to native insects if the biocontrol agent attacks nontarget species. Potential biocontrol agents are screened before release to determine their acceptance of nontarget species and the suitability of nontarget species for their development. Here we show that, even though a biocontrol agent has very low acceptance of a nontarget species, it may nonetheless have a large impact on the nontarget population. This impact does not require the nontarget species to be a suitable prey capable of supporting the biocontrol agent population, but instead may be a transient impact that occurs soon after the agent is released. Because the population of biocontrol agents is likely to increase rapidly in response to the high density of its target pest, the resulting high density of the agent population may dominate its low acceptance of the nontarget species, causing a strong decline or even local extirpation of the nontarget. We demonstrate this possibility using models of host-parasitoid dynamics that incorporate a broad range of assumptions about the life histories of hosts and parasitoids, and that demonstrate how various common aspects of host-parasitoid biology are likely to reduce this risk considerably. The predictions of the models are reasonably approximated with a simple formula, which potentially provides a simple method for assessing the risk of transient impacts, but which should only be applied loosely (in a qualitative manner) and in the context of a fuller understanding of other factors affecting risk in the system in question.

1. The harlequin bug, a herbivore on bladderpod, is attacked by two specialist egg parasitoids Trissolcus murgantiae and Ooencyrtus johnsonii. Ooencyrtus can outcompete Trissolcus in the laboratory, but coexistence is the norm in field populations. Despite the heavy mortality inflicted by the two parasitoids, the host-parasitoid interaction is persistent in all sites that have been studied in southern California. 2. I manipulated inter-patch distances in a field experiment to determine whether spatial processes drive parasitoid coexistence and/or host-parasitoid dynamics. I first tested the hypothesis that the parasitoids coexist via a dispersal-competition trade-off. Both parasitoid species took significantly longer to colonize isolated patches than well-connected patches, suggesting that they have comparable dispersal abilities. Ooencyrtus did not exclude Trissolcus even when inter-patch distances were reduced to 25-30% of those observed in natural populations. These data suggest that parasitoid coexistence can occur in the absence of a dispersal advantage to the inferior competitor. 3. Since the treatments with isolated vs. well-connected patches did not differ in parasitoid composition, I next asked whether isolation would destabilize, or drive extinct, the host-multiparasitoid interaction. No local extinctions of bugs or parasitoids were observed during the 18-month study period. Bug populations in the isolated patches were no more variable than those in the well-connected patches. In fact, temporal variability in the experimentally isolated patches was comparable to that observed in highly isolated natural populations. 4. These data argue against a strong effect of spatial processes on host-parasitoid dynamics. Local processes may mediate both parasitoid coexistence as well as the host-parasitoid interaction.