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     

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     

Parasitoid-mediated effects: apparent competition and the persistence of host–parasitoid assemblages

Indirect effects such as apparent competition (in which two hosts that do not compete for resources interact via a shared natural enemy) are increasingly being shown to be prevalent in the structure and function of ecological assemblages. Here, we review the empirical and theoretical evidence for these enemy-mediated effects in host–parasitoid assemblages. We first address questions about the design of experiments to test for apparent competition. Second, we consider factors likely to affect the coexistence of host species that share a parasitoid and are involved in apparent competition. We show that parasitoid aggregation, and the switching effect that this can generate when hosts occur in separate patches, not only promotes persistence but is also strongly stabilizing. The broader consequences of these effects are discussed. Received: November 6, 1998 / Accepted: January 13, 1999     

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.     

Population dynamics of the green leafhopper,Nephotettix virescens Distant (Hemiptera: Cicadellidae) in synchronized and staggered transplanting areas of paddy fileds in Indonesia

Summary The population dynamics ofNephotettix virescens, a vector of rice tungro virus disease was investigated in a synchronized transplanting area at Jatisari (1984–1986), West Java and in a staggered transplanting area at Sidan (1986–1988), Bali, Indonesia. The FARMCOP suction sampler was employed for population censuses ofN. virescens and its natural enemies. The population growth pattern was affected by transplanting pattern: In the staggered transplanting area, the population density increased from the immigrant generation to the first generation, and sharply decrease thereafter, while in the synchronized transplanting area the population density often reached the highest peak in the second generation. The degree of contageousness in the spatial distribution ofN. virescens was negatively correlated with population density of the immigrant generation. Contribution from Indonesia-Japan Joint Program on Food Crop Protection     

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.     

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.     

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.     

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     

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     

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     

Population and pavement: population growth and land development in Israel

This research examines land use change in Israel––an intriguing but understudied setting with regard to population–environment dynamics. While Israel is fairly unique with regard to its combined high levels of economic prosperity and high population growth, this case study has relevance for developed countries and regions (like the south and southwest regions of the USA) which must balance population growth and urban development with open space conservation for ecosystem services and biological diversity. The population–land development relationship is investigated during the period from 1961 to 1995 at three spatial scales: national, regional (six districts), and local (40 localities). There is a positive correlation between population growth and land development rates at the national scale, and while remaining positive, the strength of the relationship varies greatly at regional and local scales. The variation in population–land use dynamics across scales is used to garner insight as to the importance of geography, policy and historical settlement patterns.     

Instability,investment, disasters,and demography: natural disasters and fertility in Italy (1820–1962) and Japan (1671–1965)

This article examines whether natural disasters affect fertility—a topic little explored but of policy importance given relevance to policies regarding disaster insurance, foreign aid, and the environment. The identification strategy uses historic regional data to exploit natural variation within each of two countries: one European country—Italy (1820–1962), and one Asian country—Japan (1671–1965). The choice of study settings allows consideration of Jones’ (The European miracle, Cambridge University Press, Cambridge, 1981) theory that preindustrial differences in income and population between Asia and Europe resulted from the fertility response to different environmental risk profiles. According to the results, short-run instability, particularly that arising from the natural environment, appears to be associated with a decrease in fertility—thereby suggesting that environmental shocks and economic volatility are associated with a decrease in investment in the population size of future generations. The results also show that, contrary to Jones’ (The European miracle, Cambridge University Press, Cambridge, 1981) theory, differences in fertility between Italy and Japan cannot be explained away by disaster proneness alone. Research on the effects of natural disasters may enable social scientists and environmentalists alike to better predict the potential effects of the increase in natural disasters that may result from global climate change.     

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.     

How do Recent Population Trends Matter to Climate Change?

Although integrated assessment models (IAM) of the Intergovernmental Panel on Climate Change (IPCC) consider population as one of the root causes of greenhouse gas emissions, how population dynamics affect climate change is still under debate. Population is rarely mentioned in policy debates on climate change. Studies in the past decade have added significantly to understanding the mechanisms and complexity of population and climate interactions. In addition to the growth of total population size, research shows that changes in population composition (i.e. age, urban–rural residence, and household structure) generate substantial effects on the climate system. Moreover, studies by the impact, vulnerability and adaptation (IAV) community also reveal that population dynamics are critical in the near term for building climate change resilience and within adaptation strategies. This paper explores how global population dynamics affect carbon emissions and climate systems, how recent demographic trends matter to worldwide efforts to adapt to climate change, and how population policies could make differences for climate change mitigation and adaptation.     

The population dynamics of the large pine aphid,Cinara pinea (Mordv.)

Summary The large pine aphid,Cinara pinea lives exclusively onPinus species, where it feeds on the foliated shoots of the current and previous year. The paper describes the development of a computer model designed to simulate the aphid’s population dynamics on saplings in the controlled environment of the laboratory, i.e. in the absence of natural enemies. The model was able to account for about 80% of the variation in aphid numbers within and between trees over a three month period. Sensitivity analysis revealed that the number of pine aphids is limited primarily by nymphal emigration, the operation of which is sensitive both to density and to plant quality as reflected in aphid growth rates. Of secondary importance are changes in reproduction acting through increased reproductive delay, again a result of altered growth rates and adult size. Development, too, has an important secondary influence. Contrary to expectation and conventional belief, however, alate production proved to be of negligible importance, either in limiting or regulating population numbers. Alatae are produced in too few numbers and for too short a period to significantly alter the pattern of population change.     

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.     

One-host one-parasitoid system: Population dynamics of a zygaenid mothPryeria sinica Moore in an undisturbed habitat

Summary The population dynamics ofPryeria sinica was investigated in an undisturbed area in 1976–1979. We analyzed the process stabilizing the local population by the life table approach for immature stages and the mark-recapture method for the adult stage. Females usually layed about 130 eggs in an egg-mass. The shape of the survivorship curve was convex and was characterized by a relatively low mortality in the egg and larval stages and by a relatively high mortality in the prepupal and pupal stages. The low mortality in the early stage seemed to be not only due to the peculiar life cycle of this species (larvae develop in early spring when natural enemies are not active) but due to their protective nest-webs, larval warning coloration and repellent smell. The high mortality after cocooning was caused by severe parasitization byAgrothereutes minousubae. The number of adult in the population varied by 2.10-fold, which was less than that of other gregarious moths. The life table data and field observations suggest that adult female dispersal would have acted as a stabilizing factor, andA. minousubae as a conditioning factor on the dynamics of the moth population.