A galling aphid with extra life-cycle complexity: Population ecology and evolutionary considerations

Summary In most gall-forming aphids, only the fundatrix is able to induce a gall on the host plant. InSmynthurodes betae Westw. (and a few other species), F₂ descendants emerge from the mother gall and induce their own, morphologically different galls. This constitutes an added complexity to the already very complex life cycle of gall-forming aphids. We investigated the ecology ofS. betae on marked trees and shoots at four sites in Israel. Gall initiation, gall distribution and density, and temporal changes in clone size within the galls were investigated during two consecutive years. We discuss the possibility that the two-gall life cycle evolved from the typical one-gall system of most gall aphids, and the possible selective advantage of this added complexity in the life-history strategy of gall aphids. Although the total reproductive output ofS. betae is not higher than in related species with a single gall per life cycle, there seems to be an advantage in the subdivision of each aphid clone into several galls, thus reducing the risk of the accidental extinction of the clone (genotype) by environmental factors, including parasites and predators.     

Effects of gall volume on survival and fecundity of gall-making aphidsAdelges japonicus (Homoptera: Adelgidae)

Summary The number of larvae reaching maturity within the gall ofAdelges japonicus was positively related to gall volume, and the relationship between the number of mature larvae and gall volume did not change with different densities of colonized larvae. The population changes in the bud galls ofA. japonicus were surveyed by collecting the galls, which did not suffer predation or parasitism within the galls, from young artificial plantations ofPicea jezoensis over two years. In the year when the density of colonized larvae was high, they suffered a 42% mortality within the galls, whereas mortality was nearly zero in the low density year. The numbers of larvae per gall were positively correlated with gall volume. The regression lines of the number of colonized larvae on gall volume did not differ significantly in the regression coefficients between the two years, whereas the intercept was significantly higher in the year when the density of colonized larvae was higher. However, different within-gall mortality nullified this difference, and the regression lines of the number of mature larvae on gall volume had no significant difference both in the regression coefficients and the intercepts. This suggests that the number of mature larvae per gall was limited by available resources within the gall which were positively related to gall volume. In 25% of the galls in which mature larvae inhabited, the space within the galls were completely filled by the larvae, indicating that space was one of the limiting resources. Gall volume also affected the number of adults that emerged from the gall and the potential number of their progeny.     

Inter- and intraspecific interactions among larvae of specialist and generalist parasitoids

Intra- and interspecific larval interactions that take place in a host body were investigated for two tachnid fliesEpicampocera succincta andCompsilura concinnata (Diptera: Tachinidae) parasitizingPieris butterfly larvae.E. succincta, a specialist onPieris butterflies, showed contest-type intraspecific competition, eliminating all the other conspecific larvae. On the other hand, an extreme generalist parasitoidC. concinnata exhibited scramble-type competition, sharing the host with other conspecifics and suffering reduced body size as a result. However, when these two species occurred together in a single host,C. concinnata had a much higher chance of survival. Moreover,C. concinnata could often survive in the presence of a parasitoid waspCotesia glomerata (Hymenoptera: Braconidae) whileE. succincta could not. The high tolerance ofC. concinnata could be attributable to its being an extreme generalist: To attack and survive on many different hosts, one has to be able to deal with various competitors. The competitive inferiority of the specialistE. succincta, on the other hand, may be a result of relatively recent encounter with, those competitors.     

Preference and performance linkage in aPhyllocolpa sawfly on the willow,Salix miyabeana, on Hokkaido

A leaf-folding sawfly in the genusPhyllocolpa (Hymenoptera: Tenthredinidae) attackingSalix miyabeana (Salicaceae) was studied near Sapporo, Hokkaido, along the Ishikari River in 1993. Host plant individuals were young trees 4–7 years old which were growing rapidly, producing some long shoots with large leaves. On a gradient of shoot length classes from 0–5 cm long to over 80 cm long, shoots were much more abundant in the shorter shoot length classes. However, attacks by ovipositing females increased as shoot length increase from 0 attacks on the shortest shoots to 5.17 attacks per shoot on the longest shoots. The frequency of attack per leaf increased from 0 to 0.13 over the same range of shoot lengths. This pattern of attack resulted in a high frequency of larval establishment in feeding sites, between 0.96 and 1.00, in all attacked shoot length categories. However, probability of survival to a late instar larva increased with shoot length and corresponded to the attack pattern, indicating a preference-performance linkage between female ovipositional decisions and larval survival. The patterns found for thisPhyllocolpa species are similar for galling sawflies in North America and Europe, especially in the genusEuura, members of which make stem, bud and leaf midrib galls. Extending the pattern to aPhyllocolpa species broadens identification of pattern and ultimately the generality of the emerging theory on populations of galling sawflies.     

The effects of wild cruciferous host plants on morphology, reproductive performance and flight activity in the diamondback moth,Plutella xylostella (Lepidoptera: Yponomeutidae)

The wild crucifers,Rorippa indica andLepidium virginicum, are known to serve as host plants for the diamondback moth (DBM),Plutella xylostella, but they are less suitable than the preferred cultivated cruciferous plant, cabbage, in terms of adult body size and fecundity. The life history traits and flight activity of DBM adults grown on various host plants were investigated. The adults thus reared on each host plant were divided into three size groups (small, medium and large). In general, female adults grown on the wild crucifers were less fecund and lived longer than those reared on cabbage. Flight activity was higher in adults grown on wild crucifers than in those reared on cabbage. Male adults flew longer than females. Fecundity, longevity, flight activity and morphometrical characters of adults were positively correlated with pupal weight in individuals reared on the same host plant. A negative relationship was found between fecundity and flight activity in females of the same size group, but a positive one was observed in females reared on the same host plant.     

Seasonal host alternation by the andromeda lace bug,Stephanitis takeyai (Heteroptera: Tingidae) between its two main host-plant species

I studied the seasonal occurrence of the andromeda lace bug,Stephanitis takeyai, on its two main host-plant species. In a secondary forest in Kyoto, this bug altered its hosts seasonally, i.e., from an evergreen shrub,Pieris japonica, in winter to a deciduous shrub,Lyonia elliptica, in summer. In contrast, in Nara park where fewL. elliptica were available, the bug exploited onlyP. japonica. Thus, seasonal host alternation by this bug is not obligate. A comparison of adult longevity and fecundity on the two host-plant species demonstrated the higher quality ofL. elliptica as a food resource. Corresponding to this difference in host quality, there was a dramatic difference in the seasonal population growth in the two study sites. In Nara, the population size at the beginning of the 2nd generation was almost the same as in the overwintered generation, whereas in Kyoto the population size in the 2nd generation was approximately one hundred times as large as in the overwintered generation. Thus seasonal host alternation is adaptive for the bug. In a previous study, I reported that overwintering as eggs in living leaves of their hosts is likely to be common among all the related species of this bug. Thus, this trait can be considered to be a phylogenetic constraint to the group. I speculate that host alternation by this bug has been derived because it is more adaptive from autoecy on an evergreen plant, similar to the pattern currently found in Nara, and that this bug can not only exploit deciduous host due to a phylogenetic constraint.     

Why does onlyAthalia Japonica enter summer diapause among three sympatricAthalia sawflies feeding on crucifers?

Summary This report assesses the primary factor for the evolution of summer diapause of the three species of sawfly,Athalia japonica, A. rosae andA. infumata that feed on cruciferous plants and coexist in the same area.A. japonica has two discrete spring and autumn generations, butA. rosae andA. infumata 5–6 generations. OnlyA. japonica enters summer diapause in response to the long daylengths in spring. Although these three sawflies usually feed on the same cultivated crucifers, they differ markedly in the utilization of wild crucifers. They oviposit only on young leaves.A. japonica mainly usesCardamine plants which sprout in spring and autumn.A. rosae andA. infumata primarily use hosts with new leaves all the year round, i.e. cultivated crucifers andRorippa indica, respectively. The thermal threshold for development is lower inA. japonica than in the other two species. The low heat tolerance ofA. japonica is adapted only to cool shady habitats whereCardamine grows. Presumably, summer diapause ofA. japonica is adaptation to the deterioration of the primary host plants rather than unfavorable climatic conditions. This interpretation is supported by the movement patterns of the threeAthalia sawflies, alternative means to escape from deteriorated habitat conditions.     

Optimal clutch size of the chestnut gall-wasp,Dryocosmus kuriphilus yasumatsu (Hymenoptera: Cynipidae)

Summary Optimal clutch size of the chestnut gall-wasp,Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), was examined in galls on wild and resistant chestnut trees in 1988 and 1989. The rate of escape success of newly-emerged adults from galls was an average of 60%, irrespective of cell numbers per gall. Dry mass per cell of a gall (as an index of nutritive condition) decreased with increasing cell number per gall, but was proportional to the mean number of mature eggs of new adults per gall. The number of cells per gall that occurred most frequently did not agree with that attained by the maximum survival rate from young larva to adult emergence of the gall-wasp. This discrepancy was examined from the viewpoint of three factors: 1) quality of offspring, 2) defensive response of the host plant causing mortality of the gall-wasp before cell formation, and 3) fitness per gall vs. fitness per egg. It is concluded that the third factor is most likely to be the one best in explaining the discrepancy.     

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.     

Spatial pattern of pine wilt disease caused byBursaphelenchus xylophilus (Nematoda: Aphelenchoididae) within aPinus thunbergii stand

Summary To understand the mechanism of spread of pine wilt disease caused by the pinewood nematode,Bursaphelenchus xylophilus, which is vectored by a cerambycid,Monochamus alternatus, the spatial distribution of trees weakened by the nematode was examined within aPinus thunbergii stand from June to October for 4 years. The weakened trees were distributed in a clumped pattern in 1980 and 1981, at an early stage of infestation. In many cases, they showed a double-clumped pattern. The degree of aggregation was higher in June or July than after August. They were uniformly distributed in June or July 1982 and in June 1983 whereas they showed a double-clumped pattern after August. The trees were frequently weakened in June or July when they were near the trees weakened during the previous year. At quadrat sizes of more than 25 m², spatial overlapping was pronounced between trees weakened during June–July of the current year and those weakened in the previous year. The seasonal changes in spatial distribution of weakened trees were explained by the interaction amongM. alternatus, B. xylophilus andPinus trees.     

The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae)

A review of data on the background of wing dimorphism in carabid beetles (Coleoptera: Carabidae) and especially of the closely relatedCalathus cinctus andC. melanocephalus is given. In bothCalathus species wing dimorphism is inherited in a simple Mendelian fashion with the brachypterous condition dominant, but inC. melanocephalus the expression of the long winged genotype is under environmental control as well. The development of long winged phenotypes in the latter species is favoured by relatively favourable environmental conditions, such as high temperatures and a high food-supply. The higher fecundity of the larger and heavier long winged females of both species may compensate for losses of long winged phenotypes by flight activities. The evolutionary significance of both types of inheritance is discussed in relation to dispersal. The ‘fixed type’ as found inC. cinctus is considered an opportunistic short term ‘between sites strategy’, whereas the ‘dynamic type’ ofC. melanocephalus represents a flexible long term ‘within sites strategy’.     

Niche modification and stability of competitive systems. II. Persistence of interspecific competitive systems with parasitoid wasps

Summary Effects of niche shift in ecological time scale on the population dynamics of competing species were studied in the experimental populations of two parasitoid wasp species,Anisopteromalus calandrae andHeterospilus prosopidis (both are solitary parasites), on a host, the azuki bean weevil,Callosobruchus chinensis. Four resource conditions were set up with combination of kind of bean (azuki or black eye), and host distribution (uniform or clumped). In each resource condition, four developmental stages of hosts were provided as a resource spectrum for parasitoid wasps. Population dynamics of the two wasp populations were investigated in each resource condition in Multi-Generation Competitive Systems (MGCS), in which fresh hosts of four developmental stages were periodically introduced and were parasitized competitively by the two wasp species. Competitive coexistence of both wasps occurred in the azuki-clumped condition, where the peaks of the resource utilization curves separated in the two species; pupae inA. calandrae and the early or late fourth instar inH. prosopidis, A. calandrae was eliminated in the azuki-uniform condition andH. prosopidis went extinct in two black eye conditions irrespective of host distributions. The degrees of overlap of the resource utilization patterns of the two wasp species during population dynamics were not significantly different among resource conditions irrespective of the results of coexistence or extinction. Even in the azuki-clumped condition, however, extinction ofA. calandrae was observed when resource partitioning could not be realized with only the late fourth instar larvae available to wasps. Further analytical experiments showed that parasitizing ability ofA. calandrae increased with host density per bean with azuki beans, butA. calandrae could express higher parasitizing ability with black eye beans thanH. prosopidis irrespective of host density per bean. The flexibility in parasitizing ability byA. calandrae for various host stages under different resource conditions was thought to be the major factor in determining the competitive coexistence or the extinction of either species under different resource conditions. The present experiments also suggested that different second-best host stages between competitors could be a major contributing factor to competitive coexistence.     

How an ant decides to prey on or to attend aphids

The following results on the behavior decision making of the antLasius niger toward two species of myrmecophilous aphidsLachnus tropicalis andMyzocallis kuricola on chestnut trees have been found. (1) An individual worker consistently attended only one aphid species, even if her nestmates attended other aphid species on the same tree. (2) The ants preyed less on the aphid species which they attended than on other myrmecophilous aphid species. (3) The ants preyed less on the aphids which had been attended by their nestmates, even if both aphids were the same species. (4) The ants preyed less on aphids which had provided honeydew to their nestmates. (5) The increased aphid density per ant led to an increase in the rate of predation on the introduced aphids by the ants. These results suggest that each worker ofL. niger chooses aphid species to attend from her experience. In addition, the workers can recognize whether an aphid has been attended by their nestmates and whether an aphid has given their nestmates honeydew. Through these processes, each worker decides to attend or to prey on the aphid. As a result, they may realize efficient collective foraging dependent on aphid density per worker.     

Deme formation in gall-making aphidsAdelges japonicus (Homoptera: Adelgidae)

The deme formation hypothesis in herbivorous insects states that herbivores differentiate genetically into small demes, each specialized in the idiosyncratic traits of individual plants. We examined this hypothesis in gall-forming aphids,Adelges japonicus, by reciprocal transfers of aphids among three susceptible clones ofPicea jezoensis standing in proximity. Performance of aphids transferred to their natal clone was compared with that of aphids transferred to other novel clones. ANCOVA showed no significant donor (source of aphids) by receptor (recipient of aphids) interactions for both total aphid performance on the host tree over a life cycle and its three subdivisions(q ₁,q ₂ andq ₃). In addition, the total performance on the natal clone was lowest among those in the three clones, which was explicitly against the prediction from the local adaptation. In contrast, there were significant receptor effects onq ₁ (fecundity of gallicolae multiplied by survivorship of fundatrices while feeding on needles) andq ₃ (fecundity of fundatrices multiplied by survivorship of gallicolae before emergence from the galls), suggesting genetic differences in resistance among clones. The two-fold difference inq ₃ among clones was due to different gall size, which was highly correlated with the number of gallicolae that emerged from the gall. The two-fold difference inq ₁ seemed to be caused by different survivorship of larval fundatrices while feeding on needles.     

Movement patterns of threeAthalia sawflies in relation to the spatio-temporal distributions of their habitats

Summary I compared the differences in the movement intensity of three species of sympatricAthalia sawflies,A. japonica, A. rosae andA. infumata feeding on cruciferous plants. Mark-release-recapture census was conducted to estimate movement distance, sex ratio and age composition of adult sawflies. In addition, the sex ratio of newlyemerged adults was examined by rearing field-collected larvae until adult emergence. Age composition and longevity of adults were estimated experimentally. The movement intensity was evaluated mostly with the indirect information thus obtained. Females moved more actively than males in all three sawflies.A. japonica females of all age classes moved actively in spring and autumn, but in summer they disappeared. Also,A. rosae females of all age classes moved actively in spring and autumn. In summer, in contrast withA. japonica, A. rosae females moved most actively among the three species in all seasons.A. infumata females, in particular the young females, moved most actively among the three species, exceptA rosae in summer. The movement patterns of the three sawflies were deduced in relation to the spatio-temporal distributions of their habitats. In spring and autumn, when host plants were abundant,A. japonica andA. rosae females were dispersed among the host patches within the census are. In summer, however, when host plants were scarce,A. japonica entered diapause, whereasA. rosae migrated to neighboring areas. On the other hand,A. infumata, in particular young famale, innately dispersed to seek for temporary host plants throughout the census seasons.     

Influences of wild crucifers on life history traits and flight ability of the diamondback moth,Plutella xylostella (Lepidoptera: Yponomeutidae)

The larvae ofPlutella xylostella were fed on five wild crucifers,Capsella bursa-pastoris, Lepidium virginicum, Cardamine flexuosa, Rorippa indica, R. islandica and a crop, cabbage. The developmental period of the immature stages, adult longevity, preoviposition period, fecundity and morphometrical characters of the adults were measured. The flight activity of the adults was also measured by the tethered flight method. All the wild plants except forR. islandica were less suitable host plants than cabbage, and larvae which were fed on these less suitable plants emerged as smaller adults with shorter wings. The smaller female adults had lower fecundity but a higher flight activity. Smaller adults measured in terms of their pupal weight among individuals fed on the same host plant had longer wings. These smaller adults with longer wing flew more actively.     

Inbreeding effects on competition inTribolium

When replicate cultures ofT. confusum andT. castaneum are husbanded together under identical treatment conditions, sometimesT. confusum eliminatesT. castaneum, and other times,T. castaneum wins (i.e., competitive indeterminacy occurs). While several plausible explanations were advanced, the results of Mertz et al. (1976) implicated demographic stochasticity and not classical genetic founder effect as the predominant factor influencing the identity of the winning species. They also observed, however, that the size of the founding population had an influence on the competitive strength ofT. castaneum. The present study shows that the decline in competitive strength that accompanied decreasing founder size inT. castaneum can be amply explained by simple inbreeding depression. The eggs of inbred adults showed an approximate 15% reduction in hatchability when compared to outbred adults. No evidence was found that the decrease in competitive strength was due either to prior history differences or reduced genetic heterogeneity of the founding adults.     

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.     

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.     

Studies on the distribution pattern of the pine needle gall midge,Thecodiplosis japonensisUchida etInouye (Diptera: Cecidomyiidae) in a pine forest

Summary Numerical changes and distribution patterns of the pine needle gall midge,Thecodiplosis japonensis Uchida etInouye, were studied during the period from 1978 to 1979 in a young plantation ofPinus thunbergii in Shiga Prefecture, Japan. The survivorship curve of this species was characterized by a low mortality of larvae in galls and two high mortalities before the formation of galls and during the overwintering period in soil. The within and between-trees distributions of eggs and larvae in galls were examined by using the regression method. The egg distribution per shoot was aggregative both within and between host plants. The within-tree variations in numbers of eggs per shoot were related to the differences in the abundance of available needles for oviposition per shoot among the canopy layers. The between-tree variations reflected the heterogeneous emergence of adult females in the study plot. The degree of aggregation increased from egg to gall stage in both within- and between-tree distributions and the increase was explained by the different mortality of larvae within trees and the inversely density-dependent mortality between trees. The distribution patterns in the soil habitat stages were examined by the patchness index ( ). This species showed aggregative distributions in soil stages. There was a correlation in spatial patterns of adult emergence between the successive generations. The distribution properties of this species were discussed in connection with the population dynamics and the availability of host plants in the study plot.