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

Summary 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.     

Effects of host and parasitoid age on search behaviour and oviposition rates inLariophagus distinguendusF?rster (Hymenoptera: Pteromalidae)

Summary Oviposition rates and related behaviours were quantified forLariophagus distinguendus F?rster attackingCalosobruchus chinensis (L.) andC. maculatus (F.). Oviposition rates varied with parasitoid age; parasitoids aged 1–7 days laid approximately twice as many eggs per day as those aged 8–14 days. Similar differences were noted in search rates and handling times; younger parasitoids had higher attack rates and lower handling times than older parasitoids. Search rates and handling times also varied with the host stage available for attack. Search rates were higher and handling times were lower on larger stages. The results are discussed with reference to their impact on the dynamical behavior of insect parasitoid-host populations.     

Combining pheromone-baited and food-baited traps for insect pest control: Effects of additional control by parasitoids

Summary Two age-structured population dynamic models are analyzed in which pheromone-baited trapping and food-baited trapping are used simultaneously to eradicate an insect pest. The pest species is assumed to be under partial control by a host-specific parasitoid species. The two models assume that density-dependent population regulation is accomplished either by host larval competition or by means of oviposition interference among the parasitoids. The two trap types interact in a positive synergistic manner and this combination appears to be very promising as a useful combination of pest control methods. Several features of the system are examined; the feature which appears to cause the greatest problem is the possibility of the parasitoids being attracted to the pheromone or the food traps. In either case, the degree of attraction does not have to be very great to undermine the control effort. It is seen that food trapping becomes indispensible if host pheromone is used by the parasitoids as a host-locating kairomone. If odor in the food traps is used by the parasitoids as kairomone, then the situation appears more optimistic, as the reduction in efficiency of the food traps appears much less than with the pheromone traps when pheromone acts as kairomone.     

Effects of host age and host availability on developmental period, adult size, sex ratio, longevity and fecundity inLariophagus distinguendusF?rster (Hymenoptera: Pteromalidae)

Summary The effects of host age on parasitoid reproductive capacity are studied using the pteromalid parasitoidLariophagus distinguendus F?rster and its bruchid hosts,Callosobruchus chinensis (L.) andC. maculatus (F.). A series of experiments were performed to investigate relationships between age and size of host parasitized and the developmental period of pre-imaginal progeny, sex ratio, female size, longevity, fecundity and oviposition rate. There was no effect of host size on preimaginal parasitoid developmental period. Sex ratio varied from less than 5% females from young (small) hosts to 60% females from mature (large) hosts. Adult size, female longevity, fecundity, and oviposition rate were also positively related to host age. Females provided mature hosts lived longer than those provided either young hosts or no hosts, possibly because of an increased ability to host-feed from the larger hosts. The implications of these findings to parasitoid population reproductive capacity and host-parasitoid synchrony are discussed.     

Evolutionary character changes and population responses in an insect host-parasitoid experimental system

In an insect host (the cowpea weevilCallosobruchus maculatus)- parasitoidHeterospilus prosopidis) experimental system, the population densities of the component species oscillated for the first 20 generations and then abruptly stabilized as the parasitoid density decreased. Examination of the host and parasitoid after the 40th generation in the long-term experiment showed that (1) host larvae exhibited contest-type competition (killing other larvae inhabiting the same bean), in contrast to the founder population being scramble-type competitors and (2) the parasitoid attack rate on the host did not change. There was also an evolutionary trade-off between body size and the rates of larval survival and development, suggesting a cost of contest competition on larval survivorship and development. I tested model predictions (Tuda and Iwasa 1998) that (1) host equilibrium population size should gradually decrease as the proportion of the contest type increases and that (2) random attacks of the parasitoid on the host should reduce the rate of increase in proportion of the contest type, and the effect should become manifest especially during the first 20 generations. Two of three host-only replicates showed significant decrease in population sizes. Although the density of emerging adults per bean did not differ between replicates of the host-only and host-parasitoid systems, comparison of the host body size between them on day 270 (at the 13th generation) showed that the host was more contest-type in the host-only system than in the host-parasitoid system, as the model predicted, and later on day 650 the effect of the parasitoid had disappeared.     

Effects of parasitoid community structure upon the population dynamics of the honeysuckle leafminer,Chromatomyia suikazurae (Diptera: Agromyzidae)

Population dynamics of a leafminer,Chromatomyia suikazurae (Agromyzidae, Diptera) and its parasitoid community were studied for ten years at seven natural populations along an altitudinal gradient in Japan. This species which mines leaves of a forest shrub,Lonicera gracilipes (Caprifoliaceae), was attacked by 25 hymenopterous parasitoid species. Annually, the parasitoid community structure varied less within a population than among populations. The seven parasitoid communities were clustered into three groups corresponding to the altitudinal gradient: (a) lowland communities dominated by late-attacking, generalist pupal idiobiont eulophids and with highest species diversity, (b) hillside communities dominated by an early-attacking, specialist larval-pupal koinobiont braconid and (c) highland communities dominated by an early-attacking, generalist larval idiobiont eulophid. Annual changes of the host larval densities among the local populations were largely synchronous rather than cyclic. Among these populations, host density levels and mortality patterns greatly varied. By analyzing these inter-populational differences of host mortality patterns, the following conclusions were drawn: (1) The host mortality patterns were determined by the host utilization patterns of the locally dominant species. (2) The host pupal mortality but not larval mortality was related to species diversity but not to species richness itself of each parasitoid community. (3) Density dependence was detected only in pupal mortality at a lowland population dominated by late-attacking pupal parasitoids. These results suggest that interspecific interactions of parasitoids add additive effects to host population dynamics dissimilarly among local populations with different parasitoid communities.     

Indirect interactions in aphid–parasitoid communities

Indirect interactions between populations of different species can be important in structuring natural communities. Indirect effects are either mediated by changes in population densities (trophic or density-mediated effects) or by changes in the behavior of species that are not trophically connected (behavioral or trait-mediated effects). We reviewed the literature on aphids and their parasitoids to explore the various possible indirect interactions that can occur in such communities. The review was motivated by our study of a particular aphid–parasitoid community in a natural (i.e., nonagricultural) habitat, and by the wealth of information that exists about aphid–parasitoid systems in agricultural settings. We focused our review on aphid–parasitoid interactions, but considered how these were influenced by the other aphid natural enemies and also by aphid mutualists and host plants. We conclude that indirect effects are likely to have a major effect in structuring aphid–parasitoid communities, and that the latter are a valuable model system for testing ideas about community interactions. Received: December 20, 1998 / Accepted: January 12, 1999     

The transmission and effects of Wolbachia bacteria in parasitoids

Wolbachia bacteria are obligatory intracellular parasites of arthropods and have been detected in about 70 species of parasitic wasps and three parasitoid flies. Wolbachia are transmitted cytoplasmically (maternally) and modify host reproduction in different ways to enhance their own transmission: parthenogenesis induction (PI), cytoplasmic incompatibility (CI), or feminization (F) of genetic males. Only PI and CI are known in parasitoids. PI-Wolbachia cause thelytoky in otherwise arrhenotokous parasitoids by generating diploid (rather than haploid) unfertilized wasp eggs. CI-Wolbachia cause incompatibility of crosses between infected males and uninfected females because the paternally derived chromosomes fail to decondense and are destroyed after syngamy. More complex situations arise when hosts harbor multiple infections, which can lead to bidirectional incompatibility and may be involved in parasitoid speciation. The relative fitness of infected and uninfected hosts is important to the population dynamics of Wolbachia, and more data are needed. Evolutionary conflict should be common between host genes, Wolbachia genes, and other "selfish" genetic elements. Wolbachia-specific PCR primers are now available for several genes with different rates of evolution. These primers will permit rapid screening in future studies of spatial and temporal patterns of single and multiple infection. Molecular phylogenies show that CI- and PI-Wolbachia do not form discrete clades. In combination with experimental transfection data, this result suggests that host reproductive alterations depend on the interaction between attributes of both Wolbachia and host. Moreover, Wolbachia isolates from closely related hosts do not usually cluster together, and phylogenies suggest that Wolbachia may have radiated after their arthropod hosts. Both results support considerable horizontal transmission of Wolbachia between host species over evolutionary time. Natural horizontal transmisson between parasitoids and their hosts, or with entomoparasitic nematodes or ectoparasitic mites, remains a tantalizing but equivocal possibility. Received: November 27, 1998 / Accepted: January 15, 1999     

Host-size-dependent sex ratio in a parasitoid wasp

Charnov's host-size model explains parasitoid host-size-dependent sex ratio as an adaptive consequence when there is a differential effect of host size on the offspring fitness of parasitoid males versus females. This article tests the predictions and the assumptions of the host-size model. The parasitoid wasp Pimpla nipponica Uchida (Hymenoptera: Ichneumonidae) laid more female eggs in larger or fresher host pupae when choice among hosts of different sizes or ages was allowed. Then, whether an asymmetrical effect of host size and age on the fitness of females versus males existed in P. nipponica was examined. Larger or fresher host pupae yielded larger wasps. Larger females lived longer, whereas male size did not influence male longevity. Large males mated successfully with relatively large females but failed with small females, whereas small males could mate successfully either with small or with large females. Thus, small-male advantages were found, and this held true even under male–male competition. Ovariole and egg numbers at any one time did not differ among females of different sizes. Larger females attained higher oviposition success and spent less time and energy for oviposition in hosts. Larger females produced more eggs from a single host meal. Taken together, females gained more, and males lost more, by being large. Host size and age thus asymmetrically affected the fitness of offspring males versus females through the relationships between host size or hast age and wasp size, which means the basic assumption of the host-size model was satisfied. Therefore, sex ratio control by P. nipponica in response to host size and age is adaptive. Received: November 13, 1998 / Accepted: January 18, 1999     

Incorporating physiology into parasitoid behavioral ecology: the allocation of nutritional resources

A critical problem faced by most theoretical studies of parasitoid behavior and population dynamics has been the paucity of empirically obtained information about the pattern of resource allocation to egg production and metabolic maintenance in relation to adult diet in female parasitoids. This review calls for a shift from traditional manipulative feeding studies to studies that quantify the energetic budget of parasitoids and which take into account the dynamic nature of metabolic processes. As guidelines, we highlight the advances made along these lines with other insect groups and some of the simplest tools already available today for fulfilling this goal. Received: December 22, 1998 / Accepted: January 12, 1999     

A genetic perspective on mating systems and sex ratios of parasitoid wasps

Parasitoid sex ratios are influenced by mating systems, whether complete inbreeding, partial inbreeding, complete inbreeding avoidance, or production of all-male broods by unmated females. Population genetic theory demonstrates that inbreeding is possible in haplodiploids because the purging of deleterious and lethal mutations through haploid males reduces inbreeding depression. However, this purging does not act quickly for deleterious mutations or female-limited traits (e.g., fecundity, host searching, sex ratio). The relationship between sex ratio, inbreeding, and inbreeding depression has not been explored in depth in parasitoids. The gregarious egg parasitoid, Trichogramma pretiosum Riley, collected from Riverside, CA (USA) produced a female-biased sex ratio of 0.24 (proportion of males). Six generations of sibling mating in the laboratory uncovered considerable inbreeding depression (∼ 20%) in fecundity and sex ratio. A population genetic study (based upon allozymes) showed the population was inbred (F _it = 0.246), which corresponds to 56.6% sib-mating. However, average relatedness among females emerging from the same host egg was only 0.646, which is less than expected (0.75) if ovipositing females mate randomly. This lower relatedness could arise from inbreeding avoidance, multiple mating by females, or superparasitism. A review of the literature in general shows relatively low inbreeding depression in haplodiploid species, but indicates that inbreeding depression can be as high as that found in Drosophila. Finally, mating systems and inbreeding depression are thought to evolve in concert (in plants), but similar dynamic models of the joint evolution of sex ratio, mating systems, and inbreeding depression have not been developed for parasitoid wasps. Received: November 13, 1998 /Accepted: January 8, 1999     

Evolutionary and population dynamics of host–parasitoid interactions

The role of evolutionary dynamics in understanding host–parasitoid interactions is interlinked with the population dynamics of these interactions. Here, we address the problems in coupling evolutionary and population dynamics of host–parasitoid interactions. We review previous theoretical and empirical studies and show that evolution can alter the ecological dynamics of a host–parasitoid interaction. Whether evolution stabilizes or destabilizes the interaction depends on the direction of evolutionary changes, which are affected by ecological, physiological, and genetic details of the insect biology. We examine the effect of life history correlations on population persistence and stability, embedding two types, one of which is competitively inferior but superior in encapsulation (for parasitoid, virulence), in a Nicholson–Bailey model with intraspecific resource competition for host. If a trade-off exists between intraspecific competitive ability and encapsulation (or virulence, as a countermeasure) in both the host and parasitoid, the trade-off or even positive correlation in the parasitoid is less influential to ecological stability than the trade-off in the host. We comment on the bearing this work has on the broader issues of understanding host–parasitoid interactions, including long-term biological control. Received: November 10, 1998 / Accepted: January 18, 1999     

Dispersion analyses and resource utilization of aphid parasitoids in a non-depletable environment

Summary Dispersions and resource utilization of primary and secondary parasitoids developing in non-depletable primary host populations were determined for an aphid-parasitoid community occurring on strawberries. Analyses of dispersions based onGreen's coefficient andLloyd's Patchiness Index indicated parasitized aphids were highly aggregated initially, became less aggregated as density increased, and remained aggregated following collapse of the aphid populations. The “index of aggregation” values calculated usingTaylor's Power Law concurred with results from the other indices, and the similarity of the regression coefficients from both seasons suggests that the index of aggregation may be characteristic for communities as well as species. Analysis withIwao's regression of mean crowding on the mean generated similar results when population data were stratified temporally, and also indicated that the individual was the basic unit of the population. In a non-depletable environment, oviposition of individuals exhibiting an aggregated dispersion pattern within clumps of hosts provides primary parasitoids with a suitable trade-off between energy utilization or genetic potential, and losses associated with hyperparasitism.     

Evolution of mutualistic symbiosis: A differential equation model

In geological history, rapid speciation, called adaptive radiation, has occurred repeatedly. The origins of such newly developing taxa often evolved from the symbiosis of different species. Mutualistic symbioses are generally considered to evolve from parasitic relationships. As well as the previous model of host population with discrete generations, a differential equation model of host population with overlapping generations shows that vertical transmission, defined as the direct transfer of infection from a parent host to its progeny, is an important factor which can stimulate reduction of parasite virulence. Evolution of the vertical transmission rate from both points of view, the parasite and the host, is analyzed. There is a critical level of the rate, below which an evolutionary conflict arises (the parasite would want an increase in the rate while the host would not), and above which both species would correspond to increase the rate. Therefore, once the parasite dominates the evolutionary race so as to overcome this critical level, one-way evolution begins toward a highly mutualistic relationship with a high vertical transmission rate, possibly creating a new organism through symbiosis with perfect vertical transmission. Changes in other parameters may decrease the critical level, initiating one-way evolution. However, changes in traits, probably developed through a long interrelationship in parasitism, do not necessarily induce the evolution of mutualism. Establishment of the ability to make use of metabolic and digestive wastes from the partner certainly facilitates the evolution of mutualism, while improvements in reproductive efficiency of parasites and reduction of negative effects from exploitation in hosts on the contrary disturb mutualism.     

Temporal/spatial structure and the dynamical property of laboratory host-parasitoid systems

The effects of spatial structure in terms of local capacity, or the maximum number of larvae surviving competition at resource patches, and temporal structure in terms of the period vulnerable to parasitoid attack in host populations on the persistence of host-parasitoid systems were quantitatively evaluated by laboratory experiments and well-parameterized model analyses. One of two bruchid beetles,Callosobruchus maculatus andC. phaseoli, were used as a host with Heterospilus prosopidis used as the parasitoid.C. maculatus, in which few larvae survive competition to become adults in each bean, andC. phaseoli, in which many larvae become adults in each bean, along with two kinds of beans, the mung and the azuki, were combined to construct four (2×2) resource-herbivorous host-parasitoid systems that differed in local capacity and vulnerable period. The mung-C. maculatus system with the parasitoid was the most persistent, i.e., took the longest time for extinction of either the host or parasitoid to occur. Since this resource-herbivorous host combination exhibited the lowest local capacity and the shortest vulnerable period, these two conditions possibly promoted the persistence of the system. A model incorporating the host population structure supported the observed persistence. Furthermore, the possible contribution of the timing of density-dependent competition of the host on the host-parasitoid persistence is predicted.     

Parasitoids as model organisms for ecologists

This paper introduces the special issue of this journal, which is devoted to parasitoid ecology. We provide a brief review of the role that parasitoids have played in research in population, community, and behavioral ecology and speculate on their future importance to the subject. Received: January 11, 1999 / Accepted: January 19, 1999     

Conspecific host discrimination by ovipositingEuphydryas editha butterflies: Its nature and its consequences for offspring survivorship

Summary OvipositingE. editha butterflies display post-alighting discrimination among patches ofCollinsia torreyi, one of their major hosts in the General's Highway (GH) population at a montane site in California. Females tended to accept (i.e. oviposit on) dense patches of this host and to reject sparse patches. Possible behavioural mechanisms underlying this tendency are discussed. The consequences of this non-random pattern of oviposition for egg and larval survivorship were investigated and no differences were found in the survivorship of larvae on acceptable and unacceptable collinsias.