Oviposition and host-feeding patterns in Aphelinus asychis (Hymenoptera: Aphelinidae) at different aphid densities

Abstract. 1. The patterns of host-feeding and oviposition were examined in Aphelinus asychis Walker, which had been provided with second-instar pea aphids as hosts.
2. Female wasps responded to increasing host density (between one and forty aphids for 24 h) with an increasing tendency to oviposit rather than to feed. Superparasitism occurred at all aphid densities, even when unparasitized aphids were available.
3. Aphids intended for feeding were paralysed and died. Wasps did not feed on and oviposit in the same aphid.
4. Feeding to satiation lasted between 4 min and 42 min. Females that had starved for ≰18 h generally deposited one or more eggs before feeding again, while the reverse was true in wasps that had starved for 21 h.
5. The host-feeding behaviour of A. asychis is determined by a female's nutritional status. At low rates of host encounter, the anhydropic eggs may be resorbed. This reproductive strategy conforms to the destructive non-concurrent type among the Hymenoptera.     

A simple model of host-parasitoid interaction with host-feeding

Summary A simple mathematical model of host-parasitoid interaction with host-feeding was presented with special reference to the system of the greenhouse whitefly and the parasitoidEncarsia formosa. In the model, when a parasitoid encounters a host, it has a choice between feeding the host and ovipositing one egg in the host. It was shown that an intermediate value of the feeding ratio of all attacks gives the minimum equilibrium host density and the minimum amplitudes of fluctuation in the densities of the two species. Computer simulations of a modified model with time lags also gave the similar results. The model suggested for natural enemy introduction program that parasitoid species with host-feeding habits are promising agents for effective controls for pest insects and that the timing of introduction is very important. By an evolutionary analysis, it was shown that the feeding ratio evolves to minimize the host density under natural selection among parasitoids.     

Rate of nutrient allocation to egg production in a parasitic wasp

Recent years have seen a marked increase in our awareness of the need to incorporate greater physiological realism into studies of parasitoid behaviour and population dynamics. Quantification of the number of eggs produced as a result of a host-feeding event, the host-feeding gain, is essential for predicting when a parasitoid should bypass an opportunity for current reproduction (i.e. laying eggs) in order to feed from the host and, thus, increase its chances for future reproduction (i.e. producing further eggs). Using radioactively labelled amino acids, one of the main constituents of insect haemolymph, we followed the incorporation of a known quantity of nutrients into each individual egg laid over a long period of time relative to the average life span of the parasitoid. Although the maximum incorporation of nutrients obtained by the female from a discrete feeding event occurs within a short period of time, a large proportion of nutrients are stored and used gradually for egg production throughout the life of the parasitoid. We therefore provide novel experimental evidence showing that feeding gain is not a discrete event in time occurring shortly after feeding, as has so far been assumed, but is instead spread throughout the parasitoid''s lifetime. This has important consequences for calculating the increase in lifetime fitness as a result of a feeding event, a common currency of models that aim to predict feeding and oviposition behaviour in parasitoids.     

Adult diet affects the life history and host-killing behavior of a host-feeding parasitoid

Neochrysocharis formosa (Westwood), an important biocontrol agent of agromyzid leafminers worldwide, is a host-feeding, idiobiont parasitoid. Female wasps have three types of host-killing behaviors: reproductive (parasitism), non-reproductive host feeding (host feeding), and host stinging without oviposition or feeding (host stinging). In this study, we compared the life history and host-killing behaviors of female parasitoids under four adult diets: starvation, hosts only, hosts plus honey (10% w/v honey solution), and honey only. Furthermore, we analyzed the host-feeding and oviposition preferences of adult females in the hosts-only and hosts-plus-honey treatments. Female parasitoids feeding on hosts had significantly increased longevity, higher fecundity, more host-stinging events, and caused a higher total host mortality than parasitoids in the starvation treatment. The honey supplement significantly increased longevity, fecundity, host-stinging events, and total host mortality, as well as average daily fecundity, but did not alter host-feeding events, host-stinging events, or daily total host mortality. However, the honey supplement did reduce the number of daily host-feeding events and induced a shift toward oviposition. Finally, we found that the non-reproductive host killing caused by host feeding and host stinging enhanced the control potential of N. formosa. These results should contribute to a better understanding of the biocontrol efficiency of destructive host feeders.     

Periodicity, persistence, and collapse in host-parasitoid systems with egg limitation

There is an emerging consensus that parasitoids are limited by the number of eggs which they can lay as well as the amount of time they can search for their hosts. Since egg limitation tends to destabilize host-parasitoid dynamics, successful control of insect pests by parasitoids requires additional stabilizing mechanisms such as heterogeneity in the distribution of parasitoid attacks and host density-dependence. To better understand how egg limitation, search limitation, heterogeneity in parasitoid attacks, and host density-dependence influence host-parasitoid dynamics, discrete time models accounting for these factors are analyzed. When parasitoids are purely egg-limited, a complete anaylsis of the host-parasitoid dynamics are possible. The analysis implies that the parasitoid can invade the host system only if the parasitoid's intrinsic fitness exceeds the host's intrinsic fitness. When the parasitoid can invade, there is a critical threshold, CV*>1, of the coefficient of variation (CV) of the distribution of parasitoid attacks that determines that outcome of the invasion. If parasitoid attacks sufficiently aggregated (i.e., CV>CV*), then the host and parasitoid coexist. Typically (in a topological sense), this coexistence is shown to occur about a periodic attractor or a stable equilibrium. If the parasitoid attacks are sufficiently random (i.e. CV1. When CV<1, the parasitoid exhibits highly oscillatory dynamics. Alternatively, when parasitoid attacks are sufficiently aggregated but not overly aggregated (i.e. CV>1 but close to 1), the host and parasitoid coexist about a stable equilibrium with low host densities. The implications of these results for classical biological control are discussed.     

Migration frequency and the persistence of host-parasitoid interactions

This paper analyses the effect of migration frequency on the stability and persistence of a host-parasitoid system in a two-patch environment. The hosts and parasitoids are allowed to move from one patch to the other a certain number of times within a generation. When this number is low, i.e. when the time-scales associated with migration and demography are of the same order, host-parasitoid interactions are usually not persistent. When this number is high, however, persistence is more likely. Moreover, in this situation, aggregation methods can be used to simplify the proposed initial model into an aggregated model describing the dynamics of both the total host and parasitoid populations. Analysis of the aggregated model shows that the system reaches a stable steady state for some regions of the parameter domain. Persistence occurs when the movement of the parasitoids is asymmetrical, i.e. they move preferentially to one of the two patches. We show that the growth rate of the host population is a key parameter in determining which migration strategies of the parasitoids lead to persistent host-parasitoid interactions.     

Strange limits of stability in host-parasitoid systems

The classical Nicholson-Bailey model for a two species host-parasitoid system with discrete generations assumes random distributions of both hosts and parasitoids, randomly searching parasitoids, and random encounters between the individuals of the two species. Although unstable, this model induced many investigations into more complex host-parasitoid systems. Local linearized stability analysis shows that equilibria of host parasitoid systems within the framework of a generalized Nicholson-Bailey model are generally unstable. Stability is only possible if host fertility does not exceede ⁴=54.5982 and if superparasitism is unsuccessful. This special situation has already been discovered by Hassell et al. (1983) in their study of the effects of variable sex ratios on host parasitoid dynamics. We discuss global behaviour of the Hassell-Waage-May model using KAM-theory and illustrate its sensitivity to small perturbations, which can give rise to radically different patterns of the population dynamics of interacting hosts and parasitoids.     

A two-component model of host-parasitoid interactions: determination of the size of inundative releases of parasitoids in biological pest control

A two-component differential equation model is formulated for a host-parasitoid interaction. Transient dynamics and population crashes of this system are analysed using differential inequalities. Two different cases can be distinguished: either the intrinsic growth rate of the host population is smaller than the maximum growth rate of the parasitoid or vice versa. In the latter case, the initial ratio of parasitoids to hosts should exceed a given threshold, in order to (temporarily) halt the growth of the host population. When not only oviposition but also host-feeding occurs the dynamics do not change qualitatively. In the case that the maximum growth rate of the parasitoid population is smaller than the intrinsic growth rate of the host, a threshold still exists for the number of parasitoids in an inundative release in order to limit the growth of the host population. The size of an inundative release of parasitoids, which is necessary to keep the host population below a certain level, can be determined from the two-component model. When parameter values for hosts and parasitoids are known, an effective control of pests can be found. First it is determined whether the parasitoids are able to suppress their hosts fully. Moreover, using our simple rule of thumb it can be assessed whether suppression is also possible when the relative growth rate of the host population exceeds that of the parasitoid population. With a numerical investigation of our simple system the design of parasitoid release strategies for specific situations can be computed.     

Host-feeding and oviposition strategies of parasitoids in relation to host stage

Until now, mathematical models of parasitoid-host interactions have not incorporated the tendency for destructively host-feeding parasitoids to partition their feeding and oviposition behaviour in relation to different host stages. A literature survey reveals a trend for female parasitoids to feed preferentially or exclusively on earlier host stages and to oviposit preferentially or exclusively in/or later ones. We explore the relative advantages to host-feeding parasitoids of a number of possible host stage selection strategies. We develop hypotheses, formalizing and testing them using modifications to our earlier simulation model of host-feeding strategies (Jervis and Kidd, 1986). We conclude from our modelling that the advantage to be gained from feeding on early host stages and ovipositing in late ones is likely to be associated with: 1) reduced handling times when feeding on early stage hosts; 2) reduced wastage of progeny from mortality factors other than host-feeding by the parent parasitoid, achieved by confining oviposition to late host stages; and 3) reduced probability of progeny mortality resulting from the parent's host-feeding activities.     

Discrete-time host-parasitoid models with pest control

We propose a simple discrete-time host-parasitoid model to investigate the impact of external input of parasitoids upon the host-parasitoid interactions. It is proved that the input of the external parasitoids can eventually eliminate the host population if it is above a threshold and it also decreases the host population level in the unique interior equilibrium. It can simplify the host-parasitoid dynamics when the host population practices contest competition. We then consider a corresponding optimal control problem over a finite time period. We also derive an optimal control model using a chemical as a control for the hosts. Applying the forward-backward sweep method, we solve the optimal control problems numerically and compare the optimal host populations with the host populations when no control is applied. Our study concludes that applying a chemical to eliminate the hosts directly may be a more effective control strategy than using the parasitoids to indirectly suppress the hosts.     

Emergent neutrality drives phytoplankton species coexistence

The mechanisms that drive species coexistence and community dynamics have long puzzled ecologists. Here, we explain species coexistence, size structure and diversity patterns in a phytoplankton community using a combination of four fundamental factors: organism traits, size-based constraints, hydrology and species competition. Using a 'microscopic' Lotka-Volterra competition (MLVC) model (i.e. with explicit recipes to compute its parameters), we provide a mechanistic explanation of species coexistence along a niche axis (i.e. organismic volume). We based our model on empirically measured quantities, minimal ecological assumptions and stochastic processes. In nature, we found aggregated patterns of species biovolume (i.e. clumps) along the volume axis and a peak in species richness. Both patterns were reproduced by the MLVC model. Observed clumps corresponded to niche zones (volumes) where species fitness was highest, or where fitness was equal among competing species. The latter implies the action of equalizing processes, which would suggest emergent neutrality as a plausible mechanism to explain community patterns.     

Population outbreaks in a discrete world

We present and analyze a simple three-patch host-parasitoid model where population growth is discrete. The model gives solutions that are qualitatively similar to the stable large-amplitude patterns in space found in reaction-diffusion theory. In the context of host-parasitoid interactions, the large-amplitude portions of the solution can be thought of as spatially localized host population outbreaks. Here, we show that the biological requirements for localized population outbreaks in a discrete world are identical to those found in reaction- diffusion theory. Furthermore, the model conveniently allows investigation into the robustness of these population outbreaks under the influence of density-dependent dispersal behavior. We find that localized population outbreaks in space can still occur with modest amounts of pursuit and aggregative behavior by parasitoids. We end by showing that evidence from a real host-parasitoid system is consistent with the predictions of the model.     

Prolonged diapause and the stability of host-parasitoid interactions

We investigated the effect on host-parasitoid dynamics of prolonged diapause, a feature of the life history of many animals living in unpredictable environments, by modifying the classical May (J. Anim. Ecol. 47 (1978) 833) host-parasitoid model. We considered three patterns of development of host and parasitoid: (a) prolonged parasitoid diapause controlled by host physiology, (b) parasitoid interference in host development, preventing parasitized hosts from prolonging diapause, and (c) host diapause independent of parasitoid attack. We found that single-year prolonged diapause shifted the boundaries of the May model towards a slight increase in stability. Longer periods of diapause prolongation had a stronger influence, but this influence remained modest if we considered realistic parameter values. In contrast to other recent studies, our results suggest that prolonged diapause does not necessarily compensate for the destabilizing effects of time lags on the influence of parasitoids on population dynamics.     

Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch

Optimal host selection models based on dynamic programming predict that the physiological state of a foraging insect, i.e. egg load, energy reserves etc., influences behavioral decisions. To test this prediction, the effect of physiological state on host acceptance of the ectoparasitic wasp Agrothereutes lanceolatus was investigated. Female wasps in plastic cups (regarded as patches) were presented with hosts, and their responses to the hosts were continuously observed. After observations, the wasps were dissected and the number of mature and immature eggs they carried were counted. The results showed that behavioral decisions by the female wasps were influenced by mature egg load, but not by wasp size or immature egg load. Hence the wasps with higher egg loads were more likely to oviposit. The number of hosts previously encountered in a patch (i.e. wasp experience) also had an independent effect on females' host acceptance, indicating that female informational state was updated during foraging in that patch. Female wasps host-fed only when mature egg load approached zero. Concurrent host-feeding was not observed. Parasitoid survival was almost zero when parasitoid eggs were transferred onto hosts that were fed upon, indicating that concurrent host-feeding could cause a high degree of offspring mortality. These three results supported the assumption and prediction of optimal host-feeding models. Parasitoid host selection and host-feeding are discussed in the context of recent models.     

Life history and life table of the host-feeding parasitoid <Emphasis Type="Italic">Hemiptarsenus varicornis</Emphasis> (Hymenoptera: Eulophidae)

Hemiptarsenus varicornis (Girault), a destructive host-feeding wasp, is an important biocontrol agent/larval ectoparasitoid of agromyzid leafminers worldwide. In the present study, the life history and life table of H. varicornis reared with Liriomyza trifolii (Burgess) were studied at a constant 27 °C. The developmental durations of female and male eggs, larvae, prepupae, pupae and total immature wasps were 1.00 and 1.00, 2.57 and 2.62, 0.45 and 0.37, 3.88 and 3.52, and 7.90 and 7.52 days, respectively. This wasp showed three types of host-killing behavior: reproductive parasitization (parasitism), non-reproductive host feeding (host feeding), and host stinging without oviposition or feeding (host stinging), resulting in 133.9, 303.8, and 84.2, respectively, killed host larvae. We confirm that H. varicornis is a strong synovigenic parasitoid, with an ovigeny index of 0.003. The number of host-feeding events was strongly correlated with parasitism, host-stinging events, longevity and total host mortality. The intrinsic rate of increase, the finite rate of increase, the net reproductive rate, the gross reproduction rate, and the mean length of a generation of H. varicornis were 0.3011/day, 1.3624/day, 66.22 offspring/individual, 168.33 offspring/individual, and 13.56 days, respectively. These results could contribute to a better understanding of the biocontrol efficiency of this destructive host feeder.     

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.     

Host-Parasitoid Dynamics and the Success of Biological Control When Parasitoids Are Prone to Allee Effects

In sexual organisms, low population density can result in mating failures and subsequently yields a low population growth rate and high chance of extinction. For species that are in tight interaction, as in host-parasitoid systems, population dynamics are primarily constrained by demographic interdependences, so that mating failures may have much more intricate consequences. Our main objective is to study the demographic consequences of parasitoid mating failures at low density and its consequences on the success of biological control. For this, we developed a deterministic host-parasitoid model with a mate-finding Allee effect, allowing to tackle interactions between the Allee effect and key determinants of host-parasitoid demography such as the distribution of parasitoid attacks and host competition. Our study shows that parasitoid mating failures at low density result in an extinction threshold and increase the domain of parasitoid deterministic extinction. When proned to mate finding difficulties, parasitoids with cyclic dynamics or low searching efficiency go extinct; parasitoids with high searching efficiency may either persist or go extinct, depending on host intraspecific competition. We show that parasitoids suitable as biocontrol agents for their ability to reduce host populations are particularly likely to suffer from mate-finding Allee effects. This study highlights novel perspectives for understanding of the dynamics observed in natural host-parasitoid systems and improving the success of parasitoid introductions.     

Mathematical modelling of host-parasitoid systems: effects of chemically mediated parasitoid foraging strategies on within- and between-generation spatio-temporal dynamics.

In this paper we develop a novel discrete, individual-based mathematical model to investigate the effect of parasitoid foraging strategies on the spatial and temporal dynamics of host-parasitoid systems. The model is used to compare na?ve or random search strategies with search strategies that depend on experience and sensitivity to semiochemicals in the environment. It focuses on simple mechanistic interactions between individual hosts, parasitoids, and an underlying field of a volatile semiochemical (emitted by the hosts during feeding) which acts as a chemoattractant for the parasitoids. The model addresses movement at different spatial scales, where scale of movement also depends on the internal state of an individual. Individual interactions between hosts and parasitoids are modelled at a discrete (micro-scale) level using probabilistic rules. The resulting within-generation dynamics produced by these interactions are then used to generate the population levels for successive generations. The model simulations examine the effect of various key parameters of the model on (i) the spatio-temporal patterns of hosts and parasitoids within generations; (ii) the population levels of the hosts and parasitoids between generations. Key results of the model simulations show that the following model parameters have an important effect on either the development of patchiness within generations or the stability/instability of the population levels between generations: (i) the rate of diffusion of the kairomones; (ii) the specific search strategy adopted by the parasitoids; (iii) the rate of host increase between successive generations. Finally, evolutionary aspects concerning competition between several parasitoid subpopulations adopting different search strategies are also examined.     

Differential cannibalism and population dynamics in a host-parasitoid system

The effects of host cannibalism on a host-parasitoid system were explored through experiment and modelling. In individual encounters between parasitized and unparasitized Plodia interpunctella larvae, parasitized larvae were more likely to be cannibalized. Inclusion of this differential cannibalism into a simple Lotka-Volterra-type model of host-parasitoid population dynamics generates alternative stable states-including stable coexistence and extinction of the parasitoid — which depend on starting conditions. Possible mechanisms for differential cannibalism, and its implications for studies of host-parasitoid populations and biological control programmes are discussed.     

The usefulness of destructive host feeding parasitoids in classical biological control: theory and observation conflict

Abstract.

• 1 We examine the conventional wisdom among biological control practitioners that destructive host feeding is a desirable attribute in parasitoids employed for classical biological control, using both the predictions of population dynamics theory and historical data on biological control introductions of Hymenoptera against Homoptera.
• 2 Population dynamics theory predicts that destructive host feeders, compared with other parasitoids, are (a) either just as likely or more likely to become established, and (b) unable to depress host equilibria as strongly.
• 3 Analyses of the B IOC AT database suggest that among parasitoids of Homoptera destructive host feeders are superior to other parasitoids with respect to both establishment rate and success rate.
• 4 We present likely explanations for the disparity between the predictions of population dynamics theory and the results of database analysis. A partial explanation for the mismatch between theory and observation with respect to the degree of pest suppression may be that females of destructive host feeding parasitoids rely less upon hosts as a food source when alternative foods such as honeydew and nectar are plentiful.
• 5 We conclude that, despite the predictions of population dynamics theory, destructive host feeders are probably better biological control agents than other parasitoids, and certainly no worse, but that it would imprudent to use destructive host feeding as the sole, or even primary, selection criterion when seeking agents for classical biological control.