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.     

Population dynamics of a migrant skipper butterflyParnara guttata (Lepidoptera: Hesperiidae) II. Survival rates of immature stages in paddy fields

Summary Survival rates and mortality factors of a migrant skipperParnara guttata were censused in paddy fields in 4 localities of central and western Japan during 1975–1980, and 10 life tables were developed for 3 generations. Mortality rates of eggs, older larvae and pupae were high but those of younger larvae were very low. The high mortality rate was caused by parasitoids. Ten primary and 6 secondary parasitoids were recorded. Out of three egg parasitoids,Telenomus sp. was predominant. Larval parasitoids,Apanteles baoris andPediobus mitsukurii which are specific to genusParnara were predominant in wet land habitat, i.e. paddy land. On the other hand, tachinid flies which have a wide host range and a high searching ability were predominant in dry land habitats. Mortalities of eggs and pupae contribute more to the change in the total mortality of immature stages than those of other stages. egg parasitoids which are the major mortality factor of eggs acted density-dependently but larval and pupal parasitoids did not do so. The total mortality of immature stages occurred more or less density-dependently. Larval density on rice plants scarecely affected the survival rate of larvae.     

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     

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     

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 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.     

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.     

Prey or host searching behavior that leads to a sigmoid functional response in invertebrate predators and parasitoids

Summary Invertebrate predators and parasitoids have long been characterized as having a hyperbolic (Type 2) functional response. Modifications were made to Holling's sand paper disc experiment which consisted of limiting the initial period of search during which a host must be contacted. Failure to contact a host during this initial period causes the predator to emigrate from the search area. The modification generated a sigmoid (Type 3) functional response. This response resulted from the low probability of encountering a host during the initial period of search at low host densities in the time allotted. A limited period of search has been found in several insect parasitoids. Such a strategy would minimize the time (energy) spent per offspring produced by minimizing the time invested in searching microhabitats in which hosts are scarce or absent. The work was supported in part by NSF Grant DEB-75-04223 and by a grant from the Netherlands Dranization for the Advancement of Pure Research (ZWO).     

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.     

The role of parasitoids in evolution of habitat and larval food plant preference by three Pieris butterflies

This article attempts to explain that parasitoids provide the evolutionary pressure responsible for relationships between habitat use and larval food plant use in herbivorous insects. Three species of butterflies of the genus Pieris, P. rapae, P. melete, and P. napi use different sets of cruciferous plants. They prefer different habitats composed of similar sets of cruciferous plants. In our study, P. rapae used temporary habitats with ephemeral plants, P. melete used permanent habitat with persistent plants, although they also used temporary habitats, and P. napi used only permanent habitat. The choice experiment in the field cages indicated that each of the three butterfly species avoided oviposition on plants usually unused in its own habitat, but accepted the unused plants which grew outside its own habitat. Their habitat use and plant use were not explained by intrinsic plant quality examined in terms of larval performance. Pieris larvae collected from persistent plants or more long lasting habitats were more heavily parasitized by two specialist parasitoids, the braconid wasp Cotesia glomerata and the tachinid fly Epicampocera succincta. The results suggest that Pieris habitat and larval food plant use patterns can be explained by two principles. The evolution of habitat preference may have been driven by various factors including escape from parasitism. Once habitat preference has evolved, selection favors the evolution of larval food plant preferences by discriminating against unsuitable plants, including those which are associated with high parasitism pressures. Received: December 3, 1998 / Accepted: January 20, 1999     

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     

Host-feeding and oviposition by parasitoids in relation to host stage: Consequences for parasitoid-host population dynamics

Summary Among parasitoids which host-feed destructively, there is a tendency for females to partition their feeding and oviposition behaviour in relation to different host stages, feeding preferentially or exclusively on earlier host stages and ovipositing preferentially or exclusively in (or on) later ones. We explored the dynamic implications of this behaviour for parasitoid-host population dynamics, using modifications of the age-structured simulation models of Kidd and Jervis (1989, 1991). Using the new versions of the models, we compared the situation where parasitoids practice host stage discrimination with respect to feeding and oviposition, with the situation where they do not. Additionally, we examined the effects of host stage discrimination on populations by (a) having generations either discrete or overlapping, (b) varying initial age structure, (c) having varying degrees of density dependence acting on host adult mortality, and (d) varying parasitoid develoment times in relation to the length of host development. With either discrete or overlapping generations of the host population, a reduction in the parasitoid development time had a destabilizing influence on the parasitoid-host population interaction. With discrete generations stage discrimination had no effect on the risk of extinction, irrespective of either the degree of density dependence acting on the host population, or the initial age structure of the host population. When parasitoid search was uncoupled from the insect's adult energy requirements, the interaction was always unstable. With continuous generations, stage discrimination affected stability at certain parasitoid development times, but not at others. The relative lengths of parasitoid and host development times also influenced the tendency of the host population to show discrete or overlapping generations.     

Variations in carambola infestation rates byBactrocera carambolae drew and hancock (Diptera: Tephritidae) with fruit availability in a carambola orchard

The relationship between the infestation rate of carambola fruits byBactrocera carambolae Drew and Hancock was investigated in a carambola orchard. Phenology of the fruits was found to influence percentage infestation of fruits byB. carambolae. The proportion of unbagged or susceptible fruits infested varied with time of year and tended to decrease with the increase of unbagged fruits available on the tree. The number of ovipunctures per fruit varied with fruit size and was also found to be indicative of the number of adult insects (B. carambolae and parasitoids) that will emerge from each fruit. Higher number of susceptible fruits available on each tree also decreased both the number of ovipunctures per fruit and the number of eggs laid per fruit, which could possibly be due to the strategy of spreading the risk adopted by the femaleB. carambolae or a result of random selection with more hosts available. The main parasitoids recorded wereBiosteres vandenboschi (Fullaway) andB. arisanus (Sonan). The mean percentage of parasitism was 38.3% and it followed roughly that of infestation of fruits.     

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     

Determinants of Mortality at Older Ages: The Role of Biological Markers of Chronic Disease

Researchers have had a longstanding interest in understanding the determinants of mortality. This article examines the impact of a broad array of biological markers, together with self‐reports of physical and mental health status, on the probability of dying for older adults. The estimates are derived from logistic regression models based on data from a national survey in Taiwan. The analysis confirms previous studies demonstrating the effects of clinical measures related to metabolic syndrome on mortality and identifies detrimental effects of neuroendocrine and immune‐system markers. The results reveal that biomarkers provide independent explanatory power in the presence of self‐reported health measures. The associations between biomarkers and mortality found here provide new avenues for projecting future mortality and elucidating differences in longevity across populations.     

Accumulation of phyllodulcin in sweet-leaf plants ofHydrangea serrata and its neutrality in the defence against a specialist leafmining herbivore

Among wild plants ofHydrangea serrata (Hydrangeaceae) in Japan, there are sweet plants whose leave contain a kind of isocoumarin, phyllodulcin, which happens to be 350 times as sweet as sucrose to the human tongue. In a primary beech forest in Ashu, Kyoto, the spatial distribution of sweet plants and temporal and the spatial distribution of phyllodulcin within and among plants were investigated using a high performance liquid chromatograph. The distribution of sweet plants was confined within a valley and was parapatric with non-sweet plants. A plant's characteristic phyllodulcin accumulation did not change, even when transplanted into the different habitats. The phyllodulcin content of the sweet plants varied greatly among plants, and the population mean peaked in July when the plants flowered. Within a plant, phyllodulcin content was elevated by partial defoliation. We examined the possible effect of phyllodulcin on herbivory by a specialist leafmining herbivore,Antispila hydrangifoliella (Lepidoptera: Heliozelidae). We transplanted sweet and nonsweet plants reciprocally between their original habitats, excluded attacks by parasitoids, and compared performance of the leafminer. Leafminer colonization and larval survivorship on transplanted andin situ plants was not significantly different between sites. The fact that accumulation of phyllodulcin did not augment a defensive function, at least against herbivory by the leafminer, and the sporadic distribution of phyllodulcin-accumulating plants, suggest that the genotypes synthesizing phyllodulcin emerged independently at separate localities by mutation, and that the genotypes are almost adaptively neutral in defence against the specialist herbivore.     

A granulosis virus, possible biological agent for control ofAdoxophyes orana (Lepidoptera: Tortricidae) in apple orchards

Summary Based on the results of ecological surveys ofAdoxophyes orana and its natural enemies in apple orchards sprayed with the granulosis virus and control plots, we constructed working models to simulate the population dynamics in three different experimental plots; those treated with chemical insecticides, those with granulosis virus, and controls. The number of individuals killed by predators, parasitoids and by miscellaneous mortality factors could be calculated on the assumption of imperfect density relations; that is, relation of the number killed by each factor with the initial number of larvae was represented by a curve with an upper asymptote. We could estimate the proportion of virus infection using curves with upper asymptotes. Rate of increase from pupa to middle instar larvae of the next generation was subject to strong density-effect. Simulation we proposed in this paper suggests a possibility that a single spray of the virus at 1st generation can reduce not only the number ofA. orana larvae in the 2nd and 3rd generations but also the degree of fruits injured by this insect. Spray of chemical insecticide is considered to be ineffective in reducing the pest density and the degree of injury to low levels in subsequent generations, as compared with untreated plot, where the density of the 1st generation larvae is low.     

Mathematical model allowing the coexistence of closely related competitors at the initial stage of evolution

The mathematical model presented here aims to elucidate the essential mechanisms of coexistence of species, especially those of closely related forms, as a result of competition in the same environment. It describes a system where the fate of the competitors or mutants is observed at the initial stage of evolution. The model encompasses both the external variables and the internal state of the competitors, which differ only in one of the metabolic rate constants. Results of simulations, even with the simplified form of the model, show that stable coexistence of closely related forms in a uniform environment is possible. In addition, the model allows the analysis of the limitations on the level of differences and similarities among the competitors for achieving a state of coexistence. The essential mechanisms for the coexistence of closely related competitors are proposed to be the involvement of the metabolic network in allowing the same growth rate of competitors which have different internal states, and the interplay between the internal states of the competitors and the external variables of their environment.     

Settling-site selection and survival of two scale insects,Ceroplastes rubens andC. ceriferus, on citrus trees

Summary We studied settling-site selection and the resulting survival of two sessile scale insects,Ceroplastes rubens andC. ceriferus, in the citrus tree,Citrus unshiu, in central Japan. C. rubens preferred 0-year-old twigs most as a settling-site; the density of nymphs settling on 0-year-old twigs was significantly higher than those on ≥1-year-old twigs, and few nymphs settled on ≥3-year-old twigs. The mean survival rates from settling until reproduction in the next year were significantly higher on more preferred twigs than on less preferred ones. InC. ceriferus, nymphs significantly preferred 1- and 2-year-old twigs to 0- and ≥3-year-old ones, and the mean survival rates on the more preferred 1- and 2-year-old twigs were significantly higher than those on less preferred ≥3-year-old twigs. However, the survival rate on less preferred 0-year-old twigs was slightly higher than those on 1- and 2-year-old ones. Thus, in both species of scale, it was the preferred twigs which were more profitable sites for survival after settling, except for less preferred 0-year-old twigs forC. ceriferus. In both scale species, most mortality was due to growth cessation, which is believed to be related to the twig quality as a food source. Predators and parasitoids were minor mortality factors. Both species showed constant survival rates until the density of settled nymphs exceeded double the “upper-limit” density, whereupon they decreased drastically. Nymphs ofC. rubens settling on twigs of high scale density showed a spacing-out distribution, those ofC. ceriferus did not. InC. rubens, an increase in preference for originally less profitable twigs at the later stage of the settling season was observed, but not inC. ceriferus. Accordingly, individuals ofC. rubens showed a stronger tendency to avoid conspecifics than didC. ceriferus. Although nymphs of the two scales clearly preferred more profitable sites, their settling-site selection did not agree with the predictions from the ideal free distribution theory (Fretwell and Lucas, 1970). The discrepancies were (1) frequent settling on less profitable sites at the early stage of the settling season, (2) insufficient utilization of the most profitable twigs, and (3) virtually 100% mortality on overcrowded twigs under conditions where unoccupied profitable twigs still remained. These discrepancies are thought due to the limited dispersal time of nymphs. Contribution to the ecological studies of scale insects 2.