Host-parasitoid Population Dynamics Research Articles

Fundamental limits of parasitoid-driven host population suppression: Implications for biological control.

Parasitoid wasps are increasingly being used to control insect pest populations, where the pest is the host species parasitized by the wasp. Here we use the discrete-time formalism of the Nicholson-Bailey model to investigate a fundamental question-are there limits to parasitoid-driven suppression of the host population density while still ensuring a stable coexistence of both species? Our model formulation imposes an intrinsic self-limitation in the host's growth resulting in a carrying capacity in the absence of the parasitoid. Different versions of the model are considered with parasitism occurring at a developmental stage that is before, during, or after the growth-limiting stage. For example, the host's growth limitation may occur at its larval stage due to intraspecific competition, while the wasps attack either the host egg, larval or pupal stage. For slow-growing hosts, models with parasitism occurring at different life stages are identical in terms of their host suppression dynamics but have contrasting differences for fast-growing hosts. In the latter case, our analysis reveals that wasp parasitism occurring after host growth limitation yields the lowest pest population density conditioned on stable host-parasitoid coexistence. For ecologically relevant parameter regimes we estimate this host suppression to be roughly 10-20% of the parasitoid-free carrying capacity. We further expand the models to consider a fraction of hosts protected from parasitism (i.e., a host refuge). Our results show that for a given host reproduction rate there exists a critical value of protected host fraction beyond which, the system dynamics are stable even for high levels of parasitism that drive the host to arbitrary low population densities. In summary, our systematic analysis sheds key insights into the combined effects of density-dependence in host growth and parasitism refuge in stabilizing the host-parasitoid population dynamics with important implications for biological control.

Searching of Underground Host Patches by a Pupal Parasitoid.

When hosts are distributed in discrete patches, ways in which parasitoids search and move between patches affect variability in parasitism risk among hosts and host-parasitoid population dynamics. This study examined the patch searching behavior of the solitary pupal parasitoid Dirhinus giffardii (Silvestri) (Hymenoptera: Chalcididae) on its host Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) which pupates underground. In a series of two laboratory experiments, host patches were created by burying pupae in peat moss, and the foraging behavior of the parasitoid was recorded. If D. giffardii can detect underground patches, the parasitoid would preferentially exploit high quality patches where the quality of a patch is represented by the number of unparasitized hosts in the patch. The first experiment investigated the effect of patch size (i.e., number of hosts) and host status (whether hosts are parasitized or unparasitized) on patch searching behavior. Results showed parasitoids were more likely to exploit a large patch than a small patch regardless of host status. The second experiment examined the effect of relative locations of patches by establishing three patches (one large patch and two small patches with unequal inter-patch distances from the large patch). The probability of parasitism was lower for the small patch close to the large patch than the small patch far from the large patch. The parasitism patterns described in the experiments have important implications on the distribution of parasitism risk among hosts and population dynamics.

Stochasticity in host-parasitoid models informs mechanisms regulating population dynamics

Population dynamics of host-parasitoid interactions have been traditionally studied using a discrete-time formalism starting from the classical work of Nicholson and Bailey. It is well known that differences in parasitism risk among individual hosts can stabilize the otherwise unstable equilibrium of the Nicholson-Bailey model. Here, we consider a stochastic formulation of these discrete-time models, where the host reproduction is a random variable that varies from year to year and drives fluctuations in population densities. Interestingly, our analysis reveals that there exists an optimal level of heterogeneity in parasitism risk that minimizes the extent of fluctuations in the host population density. Intuitively, low variation in parasitism risk drives large fluctuations in the host population density as the system is on the edge of stability. In contrast, high variation in parasitism risk makes the host equilibrium sensitive to the host reproduction rate, also leading to large fluctuations in the population density. Further results show that the correlation between the adult host and parasitoid densities is high for the same year, and gradually decays to zero as one considers cross-species correlations across different years. We next consider an alternative mechanism of stabilizing host-parasitoid population dynamics based on a Type III functional response, where the parasitoid attack rate accelerates with increasing host density. Intriguingly, this nonlinear functional response makes qualitatively different correlation signatures than those seen with heterogeneity in parasitism risk. In particular, a Type III functional response leads to uncorrelated adult and parasitoid densities in the same year, but high cross-species correlation across successive years. In summary, these results argue that the cross-correlation function between population densities contains signatures for uncovering mechanisms that stabilize consumer-resource population dynamics.

Generalized stability conditions for host–parasitoid population dynamics: Implications for biological control

Discrete-time models are the traditional approach for capturing population dynamics of insects living in the temperate regions of the world. We revisit classical discrete-time models of host–parasitoid population dynamics and provide novel results on the stability of the population dynamics. Discrete-time host–parasitoid models are characterized by update functions that connect the population densities from one year to the next, and a host escape response — the fraction of hosts escaping parasitism each year. For a general class of models we show that the stability can be simply characterized in terms of two quantities: the rate at which the host equilibrium changes with the host’s growth rate, and the sensitivity of the host’s escape response to the host density. Interestingly, stability is more likely to arise when the escape response is a decreasing function of the host density rather than an increasing function. Moreover, if the host’s escape response only depends on the parasitoid population density then the stability condition is further simplified to the host equilibrium density being an increasing function of the host’s reproduction rate. We interpret several mechanisms known for stabilizing host–parasitoid population dynamics in the context of these generalized stability conditions. Next, we introduce a hybrid approach for obtaining the update functions by solving ordinary differential equations that mechanistically capture the ecological interactions between the host and the parasitoid. This hybrid approach is used to study the suppression of host density by a parasitoid. Our analysis shows that when the parasitoid attacks the host at a constant rate, then the host density cannot be suppressed beyond a certain point without making the population dynamics unstable. In contrast, when the parasitoid’s attack rate increases with increasing host density (Type III functional response), then the host population density can be suppressed to arbitrarily low levels while maintaining system stability. These results have important implications for biological control where parasitoids are introduced to eliminate a pest that is the host species for the parasitoid.

Dilution effects enhance variation in parasitism risk among hosts and stabilize host–parasitoid population dynamics

In host–parasitoid interactions, parasitism risk experienced by each host may decrease as the host density increases (referred to as the dilution effect) when parasitoids can parasitize a limited number of hosts at a given time no matter how abundant hosts are. In the relationship between parasitism risk and host–parasitoid dynamics, the dilution effect is generally considered as a destabilizing factor, whereas variability in parasitism risk among hosts is regarded a stabilizing factor. However, although the dilution effect and variability in parasitism risk have been studied in isolation, the simultaneous expression of these two factors in host–parasitoid systems has not been investigated. This study examines the dilution effect in a patchy environment using a simulation model, with a specific focus on the CV2>1 rule (which states that CV2>1 is a condition for stability where CV is the coefficient of variation in parasitism risk among hosts). The simulation model shows that the CV2>1 rule is a good predictor of stability of the model regardless of the presence or absence of the dilution effect. It was also found that the dilution effect increases CV2 and stabilizes the host–parasitoid dynamics.

Global redistribution and local migration in semi-discrete host–parasitoid population dynamic models

Host–parasitoid population dynamics is often probed using a semi-discrete/hybrid modeling framework. Here, the update functions in the discrete-time model connecting year-to-year changes in the population densities are obtained by solving ordinary differential equations that mechanistically describe interactions when hosts become vulnerable to parasitoid attacks. We use this semi-discrete formalism to study two key spatial effects: local movement (migration) of parasitoids between patches during the vulnerable period; and yearly redistribution of populations across patches outside the vulnerable period. Our results show that in the absence of any redistribution, constant density-independent migration and parasitoid attack rates are unable to stabilize an otherwise unstable host–parasitoid population dynamics. Interestingly, inclusion of host redistribution (but not parasitoid redistribution) before the start of the vulnerable period can lead to stable coexistence of both species. Next, we consider a Type-III functional response (parasitoid attack rate increases with host density), where the absence of any spatial effects leads to a neutrally stable host–parasitoid equilibrium. As before, density-independent parasitoid migration by itself is again insufficient to stabilize the population dynamics and host redistribution provides a stabilizing influence. Finally, we show that a Type-III functional response combined with density-dependent parasitoid migration leads to stable coexistence, even in the absence of population redistributions. In summary, we have systematically characterized parameter regimes leading to stable/unstable population dynamics with different forms of spatial heterogeneity coupled to the parasitoid’s functional response using mechanistically formulated semi-discrete models.

A matrix model describing host-parasitoid population dynamics: The case of Aphelinus certus and soybean aphid.

Integrating elements from life tables into population models within a matrix framework has been an underutilized method of describing host–parasitoid population dynamics. This type of modeling is useful in describing demographically-structured populations and in identifying points in the host developmental timeline susceptible to parasitic attack. We apply this approach to investigate the effect of parasitism by the Asian parasitoid Aphelinus certus on its host, the soybean aphid (Aphis glycines). We present a matrix population model with coupled equations that are analogous to a Nicholson–Bailey model. To parameterize the model, we conducted several bioassays outlining host and parasitoid life history and supplemented these studies with data obtained from the literature. Analysis of the model suggests that, at a parasitism rate of 0.21 d−1, A. certus is capable of maintaining aphid densities below economically damaging levels in 31.0% of simulations. Several parameters—parasitoid lifespan, colonization timeline, host developmental stage, and mean daily temperature—were also shown to markedly influence the overall dynamics of the system. These results suggest that A. certus might provide a valuable service in agroecosystems by suppressing soybean aphid populations at relatively low levels of parasitism. Our results also support the use of A. certus within a dynamic action threshold framework in order to maximize the value of biological control in pest management programs.

Landscape structure and agricultural intensification are weak predictors of host range and parasitism rate of cereal aphids

Proportions of specialist and generalist primary parasitoids have been described by the resource breadth and the trade-off hypothesis. These alternative hypotheses predict either decreased or increased, respectively, parasitism rate of shared aphid species by specialist parasitoids. We tested both hypotheses and the confounding effects of landscape structure and agricultural intensification (AI) using extensive samplings of aphids and their parasitoids in Polish agricultural landscapes. Abundances, species composition of aphids, primary parasitoids, and parasitism rate of aphids by specialists and generalist parasitoids were analysed. Contrary to our expectations we found equally decreased parasitism rates by both types of primary parasitoids at higher aphid densities and thus proportion of specialists to generalists did not change with increasing host density. In line with the resource breadth hypothesis, specialist parasitoids had always lower abundances and parasitism rates than generalist parasitoids. Landscape diversity and agricultural intensification did not influence the host-parasitoid population dynamics. We speculate that these contrasting results could be caused by the additional density effects of secondary parasitoids. We conclude that simplistic two-trophic-level population models are not able to fully describe the complex dynamics of trophic networks. We also argue that agricultural intensification has lower effects on abundance and effectiveness of parasitoids than predicted by respective predator–prey models and empirical studies performed in controlled and artificial conditions.

The scale and parasitoid community on native hemlocks in Japan

Elongate hemlock scale (EHS), Fiorinia externa (Hemiptera: Diaspididae), is an invasive species in the United States of Japanese origin that was first detected in New York in 1908. In the United States, EHS attacks eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana), and has established in most states where these trees occur. Elongate hemlock scale density can be several orders of magnitude higher in the United States than in its native Japan despite the presence of the parasitoid Encarsia citrina (Hymenoptera: Aphelinidae) in both locations. We postulated three possible reasons for this: (1) cryptic diversity of E. citrina attacking EHS exists in Japan, but not in the United States, (2) additional parasitoid species attack EHS in Japan at significant rates, or (3) alternate armored scale hosts on hemlock in Japan enhance rates of parasitism of EHS by E. citrina or other parasitoid species. We surveyed 88 sites (or subsites) throughout Japan for all armored scales on hemlock to explore the scale community and the genetic diversity of the associated parasitoids, as well as the relationship between scale community species richness and percent parasitism of EHS. Six armored scale species were found on hemlock in Japan. Using two gene loci (28S-D2 and COI), 18 identified or putative species of parasitoids were reared from these six armored scale species. Only five of the 18 parasitoid species were found in more than one scale host species. Eleven of the 18 parasitoid species were found in EHS, and six of these were exclusive to EHS. Encarsia citrina was recovered from all six armored scale species, and there was no evidence for cryptic species of E. citrina or that it differed genetically from populations of this species found in the eastern United States. There was no relationship between the number of armored scale species present in a given location and percent parasitism of EHS by all parasitoid species. Our phylogenetic analysis corroborated the morphological identification of the parasitoid species, including those newly described, published in an earlier study. The results from this study suggest that the high densities and low parasitism rates of EHS in the United States may be due to a depauperate scale-parasitoid community compared to Japan. In particular, this study identified ten new parasitoid species attacking EHS in Japan, which suggests strong parasitoid pressure on EHS populations there. Despite the diverse parasitoid community associated with EHS, parasitism rates were often low. This may be indicative of natural variation in spatial/temporal host-parasitoid population dynamics, scale suppression from plant-mediated factors, or a combination of both. The hemlock scale parasitoids found in this study provide many potential biological control candidates should management of EHS or other hemlock scales become necessary in the future.

Parasitoid-induced host egg abortion: An underappreciated component of biological control services provided by egg parasitoids

Accurate evaluation of the biological control services provided by insect natural enemies requires a consideration of the full diversity of means by which they can cause reductions in host or prey populations. Here, we discuss the fact that host attacks by egg parasitoids often result in failed parasitoid offspring development, while causing the host egg to abort. This parasitoid-induced host egg abortion is rarely considered explicitly, resulting in underestimations of the impact of these important biological control agents on populations of both target and non-target hosts. Two case studies are presented to illustrate the prevalence and implications of parasitoid-induced host egg abortion. The first presents a multi-species/strain dataset from the Trichogrammatidae, while considering the additional importance of host species for egg abortion rates. The second case study focuses on indigenous parasitoid attack on the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), suggesting that the degree of shared evolutionary history between parasitoids and their hosts is an important determinant of the amount of host egg abortion, that there is inter-individual variation among parasitoids of the same species for the capacity to abort host eggs, and that abortion capacity is potentially a desirable trait that could be subjected to artificial selection. We argue that parasitoid-induced host egg abortion and related forms of non-reproductive parasitoid-induced mortality could have important implications for the modeling of host-parasitoid population dynamics, the assessment of indigenous parasitoid impact following biological invasions, and host range testing of parasitoids as part of classical biological control programmes.

Variable prey development time suppresses predator–prey cycles and enhances stability

Although theoretical models have demonstrated that predator-prey population dynamics can depend critically on age (stage) structure and the duration and variability in development times of different life stages, experimental support for this theory is non-existent. We conducted an experiment with a host-parasitoid system to test the prediction that increased variability in the development time of the vulnerable host stage can promote interaction stability. Host-parasitoid microcosms were subjected to two treatments: Normal and High variance in the duration of the vulnerable host stage. In control and Normal-variance microcosms, hosts and parasitoids exhibited distinct population cycles. In contrast, insect abundances were 18-24% less variable in High- than Normal-variance microcosms. More significantly, periodicity in host-parasitoid population dynamics disappeared in the High-variance microcosms. Simulation models confirmed that stability in High-variance microcosms was sufficient to prevent extinction. We conclude that developmental variability is critical to predator-prey population dynamics and could be exploited in pest-management programs.

Comparison of the Effect of Predicted Climate Change on Two Agricultural Pest-parasitoid Systems

In insects, developmental and reproductive rates are temperature-dependent and species-specific. Therefore, the effects of climatic changes can be different for host and parasitoid species, thus changing host-parasitoid population dynamics. Within the research co-operation KLIFF (www.kliff-niedersachsen.de) we investigated the impact of climate change on selected vegetable pests and their natural enemies in Lower Saxony, Germany. As model organism we selected two important agricultural pests, Brevicoryne brassicae and Aleyrodes proletella, and their respective parasitoids, Diaeretiella rapae and Encarsia tricolor. To model the impact of predicted climatic changes on pest-parasitoid interactions age-structured simulation models were developed in INSIM1 estimating changes in population size for each species during the course of a year. Based on temperature data simulated by the climate model REMO (MPI, Hamburg, Germany) the parameters were estimated for two future time periods, 2021−2050 and 2071−2100, and compared to parameters estimated for a reference time period (1971−2000). The relative changes in maximum population size and the occurrence of population peaks for each species were analysed for the Lower Saxony area to investigate regional differences. The simulations incorporate the interactions that occur naturally between the species and allow a comparison of the impact of climate change on pest-parasitoid interactions between the time periods.

An integrative approach to understanding host–parasitoid population dynamics in real landscapes

Many of our advances regarding the spatial ecology of predators and prey have been attributed to research with insect parasitoids and their hosts. Host–parasitoid systems are ideal for spatial-ecological studies because of the small size of the organisms, the often discrete distribution of their resources, and the relative ease with which host mortality from parasitoids can be determined. We outline an integrated approach to studying host–parasitoid interactions in heterogeneous natural landscapes. This approach involves conducting experiments to obtain critically important information on dispersal and boundary behavior of the host and parasitoid, large-scale manipulations of landscape structure to reveal the impacts of landscape change on host–parasitoid interactions and temporal population dynamics, and the development of spatially realistic, behavior-based landscape models. The dividends from such an integrative approach are far reaching, as is illustrated in our research on the prairie planthopper Prokelisia crocea and its egg parasitoid Anagrus columbi that occurs in the tall-grass prairies of North America. Here, we describe the population structure of this system which is based on a long-term survey of planthoppers and parasitoids among host–plant patches. We also outline novel approaches to experimentally quantify and model the movement and boundary behavior of animals in general. The value of this information is revealed in a landscape-level field experiment that was designed to test predictions about how landscape change affects the spatial and temporal population dynamics of the host and parasitoid. Finally, with these empirical data as the foundation, we describe novel simulation models that are spatially realistic and behavior based. Drawing from this integrated approach and case study, we identify key research questions for the future.

Mitigation of egg limitation in parasitoids: immediate hormonal response and enhanced oogenesis after host use

Synovigenic insects (i.e., insects emerging with few ripe eggs and maturing more eggs during the course of their lifetime) may suffer from transient egg limitation due to the stochastic nature of encounters with patchy hosts and the low availability of ripe eggs at any given time point. Egg limitation also affects the stability of host-parasitoid models. Thus, quantification of the behavioral decisions influencing egg maturation, identification of the underlying physiological mechanisms, and determination of the rate of egg maturation are highly relevant to both parasitoid behavioral ecology and host-parasitoid population dynamics. The aim of this study was to identify, in a highly controlled setting, the physiological processes responsible for egg manufacture after varying host use by a synovigenic parasitoid. We quantified the time course of the reproductive hormonal response and subsequent egg production in the host feeding bruchid parasitoid, Eupelmus vuilleti (Hymenoptera: Eupelmidae) for three treatments: (1) host examination without further host use, (2) host feeding, and (3) host feeding followed by oviposition. We carried out continuous behavioral observations with single hosts, enzyme immunoassays for quantifying ecdysteroids, and ovary dissection. Ecdysone levels increased within two minutes of contact with a host, the fastest hormonal response reported for any insect. Even simple contact with a host, without further host use, triggered an increase in hormone levels, leading to the maturation of a single egg, using body reserves only. Feeding on the host caused a much larger increase in ecdysone levels and was followed by a marked increase in oogenesis. Oviposition had a weak effect on hormone levels, but increased oogenesis. We discuss the mechanisms responsible for these rapid responses, the source of ecdysteroids, and the implications of our results for the population dynamics of host-parasitoid systems and the behavioral ecology of synovigenic species.

Ovigeny in Selected Generalist Predators

Ovigeny refers to egg production and develop ment in adult female insects. Extremes in ovigeny yield a dichotomy: species where adults emerge with a fixed complement of mature eggs are pro ovigenic; whereas, species that display continued egg development during adulthood are (Heimpel & Rosenheim 1998). Over 98% of parasitoid species surveyed emerged with at least some immature eggs (Jervis et al. 2001). A synovi genic insect may experience short-term egg deple tion, though lifetime fecundity limitation should be rare (Carbone & Rivera 2003). Egg limitation has been demonstrated in the field, affecting host parasitoid population dynamics, possibly result ing in inverse density-dependent parasitism (Heimpel & Rosenheim 1998). Jervis et al. (2001) suggested that synovigenic species tend to be longer-lived, and that the early reproductive cost in pro-ovigenic species incurred a biological cost. Most research in ovigeny has been performed on parasitoids (mostly Hymenopterans), possibly because of the direct relationship between egg load and parasitism rates, and hence reproduc tion. However, ovigeny is a potentially unifying concept in entomology and should be applicable to all insect species (Jervis et al. 2001). Previous studies of ovigeny in insects other than parasi toids include those of Boggs (1997) in Lepidop tera. Further, Cyzenis albicans Fallen (Diptera: Tachinidae) and hoverflies in general (Diptera: Syrphidae) were determined to be synovigenic by Hassell (1968) and Gilbert (pers. comm., 1990), respectively. Legaspi & Legaspi (2004) found evi dence of strong ovigeny in Podisus maculiventris (Say) (Heteroptera: Pentatomidae) by comparing egg loads at different times during female adult hood, against lifetime fecundity in the laboratory. Limited evidence of ovigeny in P. maculiventris was also found in the field (Legaspi & Legaspi 2005). In this study, ovigeny was examined in 4 com mon generalist predators: P. maculiventris, Orius insidiosus (Say) (Hemiptera: Anthocoridae), Geo coris punctipes (Say) (Heteroptera: Geocoridae), and Delphastus catalinae (Horn) (Cole?ptera: Coccinellidae). Dissection and feeding methods for P. maculiventris are described in Legaspi & Legaspi (2004). For the O. insidiosus, G. punctipes and D. catalinae, 40 newly-emerged females of each species were selected for study and placed individually in 10-cm Petri dishes with a damp cotton ball and lined with filter paper. The Petri dishes were secured with a rubber band. A male was placed with each female throughout the ex periment except on day zero. Each Petri dish com prised 1 replicate. The 40 females were assigned to one of 4 dissection times (10 replicates each). Prey was provided ad libitum as: Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) for D. cat alinae and G. punctipes; and Ephestia kuehniella Zeller eggs and pollen. Oviposition substrates for the predators were stringbean (Phaseolus vul garis L.) for O. insidiosus and tomato (Lycopersi con esculentum Mill. syn. Solanum esculentum L.) leaf cuttings for D. catalinae and G. punctipes. Four dissection times were determined based on the expected lifespan of each species. At the be ginning of the experiment (dissection time = 0), 10 females were dissected, and the numbers of ma ture and immature eggs were recorded. At each of the remaining 3 dissection times, 10 females were dissected and examined. At each designated dis section date, total numbers of eggs laid were re corded. Numbers of mature and immature eggs were counted upon dissection. Results of dissections in P. maculiventris (Fig. 1A) showed that the numbers of immature eggs increased with the predator age, whereas the numbers of mature eggs declined (Legaspi & Le gaspi 2005) providing a clear indication of contin uous egg production during the adult stage. In the other predators that we studied, egg loads at time zero were always zero and tended to increase with time, except in D. catalinae (Fig. IB). However, the numbers of eggs laid all increased with time. Total numbers of eggs laid were higher than total egg count recorded in dissections. In O. insidio sus, 71 eggs (7.7%) were counted in dissections, versus 857 laid (92.3%). Results were similar for D. catalinae: 7 eggs (5.8%) found in dissections and 113 laid (94.2%); and G. punctipes: 189 (13.8%) versus 1183 (86.2%). These findings sug gested that egg production occurred during the adult stage in all these predators and that all predators studied were synovigenic to various de grees. In the case of D. catalinae, low egg load was likely a consequence of oviposition. Despite the fact that most studies on ovigeny have been done on parasitoids, it is not surprising that synovig eny is also common in other groups, including predators. Egg load dissections underestimate re productive potential of various species and may not be good criteria in evaluating predators as po tential biological control agents.

Modelling the spatio-temporal dynamics of multi-species host–parasitoid interactions: Heterogeneous patterns and ecological implications

A mathematical model of the spatio-temporal dynamics of a two host, two parasitoid system is presented. There is a coupling of the four species through parasitism of both hosts by one of the parasitoids. The model comprises a system of four reaction–diffusion equations. The underlying system of ordinary differential equations, modelling the host–parasitoid population dynamics, has a unique positive steady state and is shown to be capable of undergoing Hopf bifurcations, leading to limit cycle kinetics which give rise to oscillatory temporal dynamics. The stability of the positive steady state has a fundamental impact on the spatio-temporal dynamics: stable travelling waves of parasitoid invasion exhibit increasingly irregular periodic travelling wave behaviour when key parameter values are increased beyond their Hopf bifurcation point. These irregular periodic travelling waves give rise to heterogeneous spatio-temporal patterns of host and parasitoid abundance. The generation of heterogeneous patterns has ecological implications and the concepts of temporary host refuge and niche formation are considered.

Community structure and stability analysis for intraguild interactions among host, parasitoid, and predator

AbstractIntraguild predation (IGP) occurs when one species preys on a competitor species that shares a common resource. Modifying a prey–predator model with prey infection, we propose a model of IG interactions among host, parasitoid, and predator, in which the predator eats parasitized and unparasitized hosts, and the adult parasitoid density is explicitly expressed. Parameter dependences of community structure, including stability of the system, were analytically obtained. Depending on interaction strength (parasitization and predation on unparasitized and parasitized hosts), the model provides six types of community structure: (1) only the host exists, (2) the host and predator coexist stably, (3) the host and parasitoid coexist stably, (4) the host–parasitoid population dynamics are unstable, (5) the three species coexist stably, and (6) the population dynamics of the three species are unstable. In contrast to a traditional prey–predator model with prey infection, which predicts that population dynamics are always locally stable, our model predicts that they are unstable when the parasitization rate is high.

Simulated Effects of Transgenic Bt Crops on Specialist Parasitoids of Target Pests

Large-scale adoption of transgenic crops that produce Bacillus thuringiensis (Bt) toxins could greatly reduce populations of target pests and their specialist parasitoids. We used a spatially explicit model of host-parasitoid population dynamics to examine effects of Bt crops on parasitoid persistence. We modeled a 9,000-ha region with 900 fields of 10 ha, each planted with either a Bt crop or a non-Bt crop refuge. In the 13,524 simulations we conducted, the pest (i.e., host) was never lost from the region before the parasitoid. The parasitoid was lost from the region in 36% of the simulations. The host was lost after the parasitoid in 12% of all simulations. The probability of regional parasitoid loss increased as the percentage of Bt fields and rotation of field types (Bt and non-Bt) increased and as host reproductive rate and parasitoid attack rate decreased. Regional parasitoid loss also increased as the insecticide spray threshold for target pests in non-Bt fields decreased and as parasitoid susceptibility to insecticide increased. With field types fixed, regional parasitoid loss increased as parasitoid movement increased. However, with field types rotated, parasitoid movement did not influence regional parasitoid loss. Host movement did not influence regional parasitoid loss. Factors not modeled that would reduce risk of regional parasitoid loss include use of alternate hosts by the parasitoid, use of alternate host plants by the target pest, and evolution of resistance to the Bt crop by the pest. The results suggest that risk of regional parasitoid loss can be assessed from the parasitoid life history traits and reduced by increasing the percentage of refuge fields, fixing refuge locations, and increasing the insecticide spray threshold for target pests in refuges.

LIFETIME NUTRIENT DYNAMICS REVEAL SIMULTANEOUS CAPITAL AND INCOME BREEDING IN A PARASITOID

Models of host handling decisions and physiologically structured host–parasitoid 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 data-rich 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.

Perspective of practical biological control and population theories

AbstractWe have not yet had sufficient theoretical explanation for successful biological control in which a key pest is controlled after an introduction of natural enemies. I compare here real features of successful biological control and theoretical host–parasitoid population models to reduce the gap between theory and practice. I first review the historical interaction between classical biological control projects and theoretical population models. Second, I consider the importance of host refuges in host–parasitoid population dynamics as concerns the mechanisms of low and stable host density. The importance of density–dependent parasitism through parasitoid reproduction in multivoltine host–parasitoid systems and supplemental generalist natural enemies are also discussed. Finally, I consider the difference in tactics for classical biological control and for augmentation of natural enemies in annual crop systems.