Population fluctuation and persistence of one-host–two-parasitoid systems depending on resource distribution: from parasitizing behavior to population dynamics

Population dynamics and variability were examined in one-host–two-parasitoid experimental systems with different resource distributions: resource-clumped and resource-sparse conditions. The system consists of a seed beetle host, Callosobruchus chinensis, and two parasitoid wasps, Anisopteromalus calandrae (Pteromalidae) and Heterospilus prosopidis (Braconidae). In the resource-clumped condition, suitable hosts for parasitism (the late fourth-instar larvae and pupae) were clumped in 1 large resource patch, but they were scattered evenly among 16 small patches in the resource-sparse condition. Population censuses were conducted at 10-day intervals in long-term cultures, renewing 10 g of azuki beans (Vigna angularis). In both resource conditions, the first period was a single-species system of C. chinensis only, and A. calandrae was added in the second period. The one-host–one-parasitoid system with C. chinensis and A. calandrae showed stable population dynamics with small fluctuations. After addition of H. prosopidis in the third period, two of three replicates persisted to day 800 in each resource condition, although one replicate in each went to extinction at an immediate outbreak of the H. prosopidis population after the introduction. Population variabilities of C. chinensis and H. prosopidis were significantly higher and the mean population size of A. calandrae was significantly smaller in the resource-sparse condition than that in the resource-clumped one. A short-term experiment on parasitism efficiencies revealed that H. prosopidis parasitized significantly more at a low host density in the resource-sparse condition than in the resource-clumped one. Mutual interference of H. prosopidis was weak enough at low parasitoid densities but became abruptly stronger with high densities. Providing fresh hosts in a mixture of already parasitized ones, host-searching behaviors of a parasitoid were recorded by video for 3 h and were compared between the two wasp species. H. prosopidis could parasitize fresh hosts more efficiently than A. calandrae through frequent long-distance walks (walking to distant beans at one bout or outside a clump of beans with hosts and back soon on a distant bean of the clump) after reencounters with parasitized hosts. Considering all the experimental results, populations were judged to be more fragile and more likely to go to extinction in the resource-sparse condition than in the resource-clumped one. A higher attacking efficiency of H. prosopidis destabilized population dynamics more in the resource-sparse condition. Received: December 23, 1998 / Accepted: January 20, 1999     

An experimental analysis of the relationship between species combination and community persistence

Among many stabilizing factors for community dynamics, nonlinear biological interactions such as type III functional response have been widely considered to be major characteristics. However, most experimental biological communities employed so far had quite simple structures. Therefore, the possibility that the conclusions in earlier studies were dependent on simple community structure is undeniable. In this study, using a multiple-species experimental community, we evaluated which combinations of component species and what kinds of interspecific interactions allow communities to persist and how these contribute to community persistence. We conducted experimental communities using two species of beans, the adzuki bean (Vigna angularis) and the red kidney bean (Phaseolus vulgaris), two species of bean weevils, the Mexican bean weevil (Zabrotes subfasciatus, Coleoptera: Bruchidae) and adzuki bean weevil (Callosobruchus chinensis, Coleoptera: Bruchidae), and two species of parasitic wasp, Heterospilus prosopidis (Hymenoptera: Braconidae) and Anisopteromalus calandrae (Hymenoptera: Pteromalidae). The outcome of multiple-generation experimental communities was explained by the characteristics of component species obtained from short-term experiments. In our two resources–two herbivores–one carnivore system, the strong density-dependent attack ability of one parasitic wasp species (A. calandrae) led to the extinction of C. chinensis. On the other hand, the weak density-dependent attack ability of the other parasitic wasp species (H. prosopidis) led to system persistence. Our overall results show that, in a multiple-species community, the combination of species itself is more important for community persistence than are the characteristics of the particular species. Received: September 29, 1997 / Accepted: October 5, 1998     

Niche modification and stability of competitive systems. III. Simulation model analysis

Summary Simulation model for niche shift in ecological time scale was constructed on the basis of the optimal foraging theory. In accordance with the previous experimental study (Shimada andFujii, 1985), the model competitive system consisted of 2 parasitoid wasp species utilizing 4 host stages. Wasps were assumed to choose host stages in the manner that they realized the maximal gain/cost values, where gain was represented by body weight of a wasp progeny emerging from each host stage and cost was expressed by time required to search for and detect an unparasitized host. The number of parasitized hosts in each host stage was calculated numerically by usingArditt's (1983) model for avoidance of superparasitism. The model simulated well the experimental results ofShimada andFujii (1985) andShimada (1985). Sensitivity analysis of the model showed that the experimentally derived criterion for competitive coexistence (different second-best host stages between competing species even with the common best) was not necessarily the indispensable condition for niche shift and separation, but that if the criterion was not satisfied, stable competitive coexistence occurred only in the narrow range of the parametric values. Further, niche shift in ecological time scale made the competitive coexistence more stable than fixed niche on which the current niche theory stands.     

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.     

Differential diet breadths and species coexistence in leafroller-hunting eumenid wasps

Summary There are, at least, three possible ways in which similar species coexist; resource partitioning, interference competition, and exploitation competition. Here, I investigated which way contributed to the coexistence of leafroller-hunting eumenid wasp species. Resource partitioning and, in addition, differential diet breadths proved to promote species coexistence in this case. First, I analyze the prey records and diet overlap of four eumenid species in a local area. The larger two eumenids hunted similar-sized prey items and had similar potential taxonomic prey uses. But the diet breadth of the subsocial eumenid was much wider than that of the solitary one. As a result, the diet overlap between the two large eumenids decreased. This was because the solitary eumenid attend repeatedly to the same hunting site inhabited by one abundant prey species, while the subsocial one made random hunting. On the other hand, the two medium-sized eumenids partitioned resources according to prey size. Secondly, I related these results to prey choice by several other species of eumenid obtained from literature sources. Ten Japanese common eumenids were divided into four groups according to their prey size. In each of the four groups, 2 to 3 wasp species differentiated the habitat (1 group) or coexisted by means of differential diet breadths (parallel with differential sociality, 2 groups). Contribution to the ecological studies of the eumenid wasps. III.     

The effects of spatial and temporal environmental heterogeneities on persistence in a laboratory experimental community

Among many stabilizing factors for community dynamics, spatial and temporal heterogeneities have been widely considered in recent years as two of the most important properties. However, the difference between the two types of heterogeneities have not been studied, except for Clark and Yoshimura (1993). We evaluated experimentally the effect of temporal and spatial heterogeneities on the persistence of a biological community. The experimental communities consisted of one parasitic wasp species, one bean weevil species, and two kinds of bean. Temporal and spatial heterogeneities of experimental communities were generated by kinds and timing of bean supply. Of all the experimental communities, the most persistent community was a temporally and spatially homogeneous community with Red Kidney bean as primary resource. Compared to spatially heterogeneous communities, temporally heterogeneous communities were more persistent. These results were easily explained by considering the attack rate of parasitic wasps and the difference between arithmetic and geometric means. In order to discuss the relative importance of environmental heterogeneity and the mode of biological interaction on community persistence, we have to measure the degree of environmental heterogeneity as the rate of change of the strength of interspecific interactions.     

Frequent successful multiparasitism by five parasitoids attacking the scale insectNipponaclerda biwakoensis

Successful multiparasitism by five parasitoid wasps of the scale insectNipponaclerda biwakoensis was investigated at a reed bed in Lake Biwa. The wasps were gregarious endoparasitoids consuming the entire body of the host. The rate of successful multiparasitism for a parasitoid species was defined as the proportion of the number of individual hosts from which the species emergedwith other species to the total number of hosts from which the species emerged. The rates were high for each parasitoid species, ranging from 17 to 82%. Successful multiparasitism frequently involved two species with similar adult size, but rarely involved species with different adult size. For four of the five species, the number of wasps per host was significantly less when wasps emerged from a host with other species relative to when emerged alone. For the other one species, the number of wasps was less, but the difference was not significant. With only one species, female wasps were significantly smaller when they emerged from a host with other species relative to when emerged alone.     

Population-level analysis on reduction in equilibrium population size of the azuki bean beetle

Summary Responses of laboratory population of the azuki bean beetleCallosobruchus chinensis to temperature conditions of 30°C and 32°C are compared. Equilibrium population size was found to be lower at 32°C. A one-generation process examined by reproduction-curve experiments is divided into two consecutive life stages specified by different habitats, i.e., outside and inside beans. Modified logistic difference equations are used to describe these population-level responses at each life stages. Sensitivity analysis is used to determine parameters of importance, thus determining the main cause of the reduced equilibrium population size at 32°C. The reduction resulted from the decrease in maximum population size of emerged adults which have experienced inside-bean process. The application and limitation of this population-level analysis to different levels 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.     

Persistence of a fig wasp population and evolution of dioecy in figs: a simulation study

The relationship between fig trees and their pollinator wasps is a well-known example of species-specific obligate mutualism. In this article we present a stochastic model of this mutualistic system, referring to data on a dioecious fig (Ficus schwarzii) in Borneo, and examine the conditions for the persistence of a wasp population for a given period. (1) When the average duration of the flowering interval of fig trees is short, even a small fig population can sustain a wasp population successfully. A population whose average period of flowering cycle is half that of another population can sustain a wasp population with a number of trees less than half of the other population. (2) The wasp survival rate (WSR) is higher when (a) the variation of the interval periods of fig flowering is smaller, (b) the fig population size is larger, and (c) figs can prolong their receptivity to wait for a wasp if no wasps are available. (3) WSR is predictable from the average proportion of the fig's receptive phases, in which wasps are available, to their total receptive phases. (4) The persistence period of a wasp population increases exponentially with the number of fig trees. Based on these results we propose a new hypothesis, as a possible scenario, on the evolution of dioecy from monoecy in Ficus. Received: November 13, 1998 / Accepted: July 14, 1999     

Searching preference of the parasitoid,Anisopteromalus calandrae (Howard) for different stages of the host,Callosobruchus maculatus (F.) in the laboratory

Summary The functional response parameters of the parasitoid,Anisopteromalus calandrae (Howard) to the third instar, the fourth instar and the pupae ofCallosobruchus maculatus (F.) were estimated from the Random Parasitoid Equation. By modifying this equation for a two host situation and using the parameters estimated above, a no switch model could be obtained. This model was then used to test for switching. In the preference experiments where two stages of the host were presented to the female parasitoid, a definite preference for the fourth instar followed by the pupa and the third instar, respectively was shown. There was, however, no evidence of switching. There was also no evidence that the data fitted the no switch models which suggests that when the parasitoid is searching in an environment with two or more hosts, its searching behaviour is more complex.     

Contest and scramble competitions in two bruchid species,Callosobruchus analis andC. Phaseoli (Coleoptera: Bruchidae)

Summary We performed multiple-generation competition experiments betweenCallosobruchus analis andC. phaseoli with different bean sizes. In each system, we supplied 5 g of mung beans (Vigna radiata) every 10 days. We examined three types of bean conditions: 5 g of large beans, 5 g of small beans, and a mixture of 2.5 g of large and small beans. In small bean condition,C. analis dominatedC. phaseoli in all three replicates andC. phaseoli was extinct by the 260th day. On the contrary,C. phaseoli overcameC. analis within 250 days in large beans in all three replicates. In mixed beans condition the two bruchid species coexisted more than 500 days in two out of the three replicates. Even in the exceptional case, both species coexisted for 460 days. These results were examined in the light of the predictions from short-term larval competition experiments and a game theoretical model by Smith and Lessells (1985). The density and frequency dependent results during larval competition inside a bean was concluded to be a main factor to produce the above long-term competition results.     

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     

Coexistence and weak amensalism of congeneric gall-forming aphids on the Japanese elm

Closely related species of gall-forming aphids are often associated with a single host species. SixTetraneura species coexist on the Japanese elm,Ulmus davidiana, in Sapporo, northern Japan. This paper describes the probabilities of coexistence on macro- and microgeographic scales (i.e., on host trees and host leaves) and examines whether coexistence with conspecific or heterospecific galls on leaves or shoots has any effect on the fecundity of each aphid species using multiple regression. A Monte Carlo simulation showed that the frequency distribution of the numbers of species on individual host trees differed significantly from that expected from the null model. There were significantly positive or negative associations between species.Tetraneura radicicola andsorini always coexisted with other species on trees they infested. Multiple regression revealed that the coexistence of conspecific or heterospecific galls on individual leaves had no influence on the fecundity ofradicicola andsorini, but had a negative influence on that of sp. O. On average,radicicola andsorini produced a smaller number of offspring in galls than sp. O, and obviously consumed only a small part of resources available on the galled leaves. Evidence available suggests that although amensalism does arise between sp. O and other species, its influence in not so strong as to exclude sp. O competitively from theTetraneura community.     

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     

Competitive exclusion through reproductive interference

Summary A simple differential equation model was developed to describe the competitive interaction that may occur between species through reproductive interference. The model has the form comparable to Volterra's competition equations, and the graphical analysis of the outcome of the two-species interaction based on its zero-growth isoclines proved that: (1) The possible outcome in this model, as in usual models of resource competition, is either stable coexistence of both species or gradual exclusion of one species by the other, depending critically upon the values of the activity overlapping coefficientc _ij ; (2) but, for the samec _ij -values, competitive exclusion is much more ready to occur here than in resource competition; (3) and moreover, the final result of the competition is always dependent on the initial-condition due to its non-linear isoclines, i.e., even under the parameter condition that generally allows both species to coexist, an extreme bias in intial density to one species can readily cause subsequent complete exclusion of its counterparts. Thus, it may follow that the reproductive interference is likely to be working in nature as an efficient mechanism to bring about habitat partitioning in either time or space between some closely related species in insect communities, even though they inhabit heterogeneous habitats where resource competition rarely occurs so that they could otherwise attain steady coexistence.     

The dynamics of laboratory populations ofCallosobruchus chinensis andC. Maculatus (Coleoptera: Bruchidae) in patchy environments

Summary Experiments are described showing the long-term dynamics of two species of bruchid beetles (Callosobruchus chinensis andC. maculatus) in arenas in which the resource of 50 black-eyed beans is divided between 5, 10 or 50 ‘patches’. Both species of adult beetles exhibit clumped distributions between patches. Within a patch there is a tendency for a density dependent reduction in (1) eggs laid per female, (2) the proportion of eggs hatching per bean (C. chinensis only) and (3) larval survival which is strongly overcompensating (particularly inC. maculatus). A discrete generation model is used as a framework to draw these results together and show how the different factors affecting natality and mortality can influence the population dynamics. Finally, the importance of the resource renewal interval in influencing the period of the population cycles is discussed.     

Pollination and factors limiting fruit set of chasmogamous flowers of an amphicapric annual,Polygonum thunbergii (Polygonaceae)

Summary We observed phenology and insect visitors of chasmogamous flowers of an amphicarpic annual,Polygonum thunbergii (Polygonaceae) in Kyoto, Japan, and clarified limiting factors for fruit set by bagging and hand-pollination experiments. Flowering season was one month from late September. Flowers were visited by various insect groups (total 30 families and 64 species) and effective pollinators were lower bees (Halictidae) and wasps (Vespidae) in the early flowering season, and middle-sized flies (Syrphidae and Calliphoridae) in the later season. Nectar was secreted at a constant rate (0.013mg sugar/hour) throughout a day and >90% of it was consumed by insects. The average number of flowers per ramet was 122, of which 95% were pollinated in the natural conditions. Bagging experiments showed that 47% of flowers were self-pollinated even under no pollinator visits. Despite of a high probability of cross pollination, the probability of fruit set within the ramet was 0.30 due to resource limitation. We discussed possible adaptive significance of cleistogamous flowers under the condition that seeds could be produced by chasmogamous flowers through self-pollination even under pollinator limited conditions.     

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     

Comparison of life tables between the solitary eumenid waspAnterhynchium flavomarginatum and the subsocial eumenid waspOrancistrocerus drewseni to evaluate the adaptive significance of maternal care

Summary I compared life tables between the solitary eumenid waspAnterhynchium flavomarginatum Smith and the subsocial eumenid waspOrancistrocerus drewseni Saussure in Kyoto, Japan, during 1980–1983. The subsocial eumenid is parthenogenetic in this study area. There were 9 identified mortality factors in the solitary eumenid and 7 in the subsocial eumenid, 6 of which were common to the two eumenids. The important differences of mortality between the two eumenids were seen in the egg, larval, and prepupal stages. In the egg stage, mortality by the phorid flyMegaselia sp. was much lower in the subsocial eumenid (1.4%) than in the solitary eumenid (15.0%) likely because of the matenal care of the subsocial eumenid (progressive provisioning and other related behavior), which reduced predation pressure. In the larval stage, mortality by the miltogrammine flyAmobia distorta was also lower in the subsocial eumenid (8.1%) than in the solitary eumenid (23.8%) also probably because of the maternal care of the subsocial eumenid. A comparison of mortality in the two eumenids between the stable, long continuing natural nest sites and the additional temporal ones showed that the phorid fly remained near its birth place and parasitized stable nest sites. The miltogrammine fly followed returning eumenid wasps and parasitized those nest sites that have a high host density. In the prepupal stage, mortality by endogenous death was higher in the subsocial eumenid than in the solitary eumenid. Mortality due to the rhipiphorid beetle was also higher in the subsocial eumenid probably due to more frequent flower-visits by the subsocial eumenid. The defense mechanism of the subsocial eumenid was discussed in relation to the evolution of subsociality. Contribution to the ecological studies of the eumenid wasps. I.