Effects of nematode parasitism on mycophagous drosophilid species in northern Japan

Mycophagous drosophilids and their nematode parasites were studied in an intensive census conducted throughout the active season over four years (2000–2003) in Hokkaido, northern Japan. Using census data, I assessed the prevalence of nematode parasitism through seasons, determined its effects on drosophilid female fertility and tested the “disproportionate parasitism hypothesis” to evaluate its effects on drosophilid community structure. Over the four‐year census, a total of 43 fungal species were found on the census route and 18 177 adult drosophilid flies were collected. The yearly parasitism rate on the total drosophilid community varied from 6.2% in 2000 to 5.1% in 2001 and 3.0% in 2002 and 2003. There was strong seasonal variation in the prevalence of parasitism. In addition, parasitism rates varied among drosophilid species. All parasitized females carried only small numbers of eggs. Thus, nematode parasitism had a strong deleterious effect on the fitness of infected flies. The relative abundance of drosophilid species and parasitism rate were not significantly correlated. Thus, the disproportionate parasitism hypothesis likely does not apply to the mycophagous drosophilid community in Japan.     

Diversity and host associations of parasitoids attacking mycophagous drosophilids (Diptera: Drosophilidae) in northern and central Japan

The diversity and host associations of parasitoids attacking mycophagous drosophilids were studied in Tokyo (a warm‐temperate region) and Sapporo (a cool‐temperate region) in Japan. Field collections were carried out using traps baited with mushrooms in May, June, September and October 2009 in Tokyo and in July and August 2010 in Sapporo. The major drosophilid species that emerged from mushroom baits was Drosophila bizonata in Tokyo and D. orientacea in Sapporo. In total, 13 parasitoid species emerged from drosophilids occurring in mushroom baits, and 11 of them were larval parasitoids belonging to Braconidae and Figitidae. Among the 11 larval parasitoids, 10 were collected in Tokyo, while only two were collected in Sapporo. It is not known why their diversity differed so much between these two regions. Four of the 11 larval parasitoids have also been recorded from drosophilid larvae occurring in fruit (banana). The use of these two habitats (mushrooms and fruit) by these four species seems to reflect the occurrence (i.e. resource use) of their suitable hosts. On the other hand, most larval parasitoids from Tokyo attacked D. bizonata, and two larval parasitoids from Sapporo attacked D. orientacea, suggesting that the abundance of potential hosts is one of the important factors affecting their host use.     

Community dynamics of leafminers (Diptera: Agromyzidae) and their parasitoids (Hymenoptera) in a natural habitat from Central Argentina

We examined the temporal community dynamics of leafminers (Agromyzidae: Diptera) and their mainly polyphagous parasitoids in a natural habitat from Central Argentina. Changes in community composition are shown by changes in dominant species and similarity coefficients. Abundance of leafminers was highest in winter, and was not related to their species richness. Abundance and species richness were correlated in the parasitoid community. Temporal variation in parasitoid diversity and abundance were positively correlated with species number and density in the host community. Apparent parasitism was greater when parasitoid species richness was high and parasitoid community dominance was low.     

The role of host plant species in the phenotypic differentiation of sympatric populations of Aleiodes nolophanae and Cotesia marginiventris

The ecology of parasitoids is strongly influenced by their host plant species. Parasitoid fitness can be affected by a variety of plant traits that could promote phenotypic differentiation among populations of parasitoids. Generalist parasitoids are expected to be more affected by plant traits (e.g., plant defensive traits) than specialist parasitoids. Data are presented on phenotypic differences of two braconid parasitoid wasps ovipositing on the same insect host species on two different host plant species. Adult mass, adult longevity, and percent parasitism are compared for the generalist parasitoid Cotesia marginiventris Cresson and the specialist parasitoid Aleiodes nolophanae Ashmead (both Hymenoptera: Braconidae) emerging from green cloverworms, Hypena scabra Fabricius (Lepidoptera: Noctuidae), feeding on two host plant species, alfalfa (Medicago sativa L.) and soybean (Glycine max L. Merr.) (both Fabaceae), at three locations. Specialist wasps that parasitized the green cloverworm on alfalfa had a significantly larger mass than the ones that parasitized the green cloverworm on soybean at the three study sites. Generalist wasps that parasitized green cloverworms on alfalfa had a larger mass than wasps parasitizing green cloverworms on soybean only at one of the study sites (i.e., Prince George's County, MD, USA). Similarly, both specialist and generalist wasps lived longer when parasitizing green cloverworms on alfalfa than when parasitizing them on soybean at only one of the study sites (i.e., Prince George's County). In Prince George's County, percent parasitism on alfalfa by the specialist parasitoid was higher than on soybean for three consecutive years and percent parasitism by the generalist parasitoid was the same on alfalfa and soybean every year. Thus, phenotypic differences among populations associated with different host plant species vary geographically (i.e., parasitoid phenotype associated with different host plant species differ at some sites while it is the same at other sites). The implications of geographic variation for biological control are discussed.     

Nematode parasitism in a Danish drosophilid community: further evaluation of the disproportionate parasitism hypothesis

The nematodes Parasitylenchus diplogenus and Howardula aoronymphium (Allantonematidae) are parasites of drosophilids (Diptera). Nematodes were found in 3/14 drosophilid species sampled in Danish woodlands: Drosophila phalerata Meigen (3.5% parasitism) was parasitized by H. aoronymphium and D. obscura Fallén (0.5%) and D. subobscura Collin (2.1%) by P. diplogenus. Parasitism was generally rare, and few drosophilid species parasitized, compared to elsewhere in Europe. Parasitism was positively correlated with relative host abundance both within Denmark and across communities, suggesting that species diversity is promoted by a disproportionately high parasitism of more common host species. The prevalence of H. aoronymphium, but not P. diplogenus, parasitism is positively related to temperature across communities.     

The Distributions of Parasitoids (Hymenoptera) of Anastrepha Fruit Flies (Diptera: Tephritidae) along an Altitudinal Gradient in Veracruz, Mexico

In the state of Veracruz, Mexico, fruits from 38 sites at various altitudes were collected monthly over a period of 2 years, and the tephritid fruit flies of the genus Anastrepha and associated parasitoids that emerged from these fruits were identified and counted. Of the 26 species of fruits that contained Anastrepha larvae, 18 species also contained a total of 10 species of Anastrepha parasitoids. These consisted of 4 native and 1 exotic species of opiine braconid larval–pupal parasitoids, 2 native species of eucoilid larval–pupal parasitoids, 1 exotic species of eulophid larval–pupal parasitoid, 1 exotic species of pteromalid pupal parasitoid, and 1 native species of diapriid pupal parasitoid. Overall parasitism (including flies from fruit species that bore no parasitoids) was 6% and was greatest, 16%, at 600–800 m in altitude. The relative contributions of individual parasitoid species to overall parasitism were frequently influenced by both the altitude (and correlated changes in temperature and precipitation) and the species of plant in which the Anastrepha larvae were found. This was particularly the case among the more abundant and widespread Braconidae. To distinguish the role of altitude from that of the distributions of the host plants, these braconids were examined in 4 individual species of fruit that grew over a broad range of altitudes. In guava (Psidium guajava L.) and “jobo” (Spondias mombin L.) the parasitoid Doryctobracon areolatus (Szepligeti) was relatively more common at low altitudes. Its congener, Doryctobracon crawfordi (Viereck), was relatively more abundant at high altitudes in sour orange (Citrus aurantium L.). Utetes anastrephae (Viereck) became relatively more common at higher altitudes in S. mombin, whereas Diachasmimorpha longicaudata (Ashmead) tended to become relatively rare at the highest altitudes in C. aurantium, but increased at high altitudes in P. guajava compared to other braconids. Different altitudinal patterns of abundance in different fruits suggests the importance of both biotic and abiotic factors in parasitoid distributions. We discuss the effect of an expanding agricultural frontier on parasitoid abundance and relate our findings to the design of a fruit fly biological control program that tailors mass releases to parasitoid climate preferences.     

Nematode parasitism in a northern European drosophilid community

Many factors may influence the structure of invertebrate communities. Among these is the presence of parasites which attack some or all members of a guild and potentially promote coexistence of competitor species. We assessed the prevalence of nematode (Allantonematidae) parasitism in Dutch woodland drosophilids (Diptera). Nematodes were found in 6 of the 18 drosophilid species sampled (percentage parasitism in parentheses): Drosophila phalerata (16%), D. kuntzei (5.1%), D. immigrans (0.5%), D. testacea (1.2%) and D. transversa (2.8%) were all parasitized by Howardula aoronymphium and D. subobscura (3%) was parasitized by Parazitylenchus diplogenus. This is the first report of nematode parasitism of D. immigrans and D. transversa. There were no important seasonal trends in percentage parasitism. We explored the consequences of nematode parasitism for individual drosophilids. Nematodes did not exert an important influence on the wing length (adult body size) of the drosophilids we sampled, but egg loads (fecundities) of female D. phalerata, D. subobscura and D. kuntzei were reduced by nematode parasitism. Parasitism rates were positively correlated with relative host abundance, in Dutch and other communities, suggesting that species diversity is promoted by a disproportionately high parasitism of more common host species.     

Population dynamics of Thecodiplosis japonensis (Diptera: Cecidomyiidae) under influence of parasitism by Inostemma matsutama and Inostemma seoulis (Hymenoptera: Platygastridae)

To understand influence of two species of parasitoids on host population dynamics, adult population dynamics of pine needle gall midge (PNGM), Thecodiplosis japonensis and two species of parasitoids, Inostemma matsutama and Inostemma seoulis were observed using emergence traps from 1986 to 2005. Density of PNGM decreased after outbreaks in 1986 and 1987 and showed density-dependent regulation. Relationships between density of PNGM and its parasitoids were linear except the period of outbreak regardless of parasitoids species. Relationships between host density and parasitism of I. matsutama and I. seoulis were density-independent and inverse density-dependent, respectively. I. seoulis was the dominant parasitoid against PNGM. Interspecific competition between two parasitoids was not strong and temporal niche segregation between two parasitoids was a possible mechanism for coexistence of two parasitoids. The parasitoid complex responded to changes in host density more sensitively than single parasitoid species. These results suggested that two parasitoid can stabilize PNGM population density without strong negative effects on each species of parasitoids.     

Weak parasitoid-mediated apparent competition between two Phyllonorycter (Lepidoptera: Gracillariidae) leaf miner species on a deciduous oak Quercus dentata

Parasitoid assemblages and the rates of parasitism on tissue-feeding larvae of two Phyllonorycter leaf miner species, P. persimilis and P. leucocorona , were studied from the autumn generation in 2002 to the summer generation in 2005 to understand whether parasitoids mediate interactions between the two leaf miner species. Fourteen species of parasitoids emerged from P. persimilis and 11 emerged from P. leucocorona . The parasitism rate was high: 24.1–92.6% in P. persimilis and 58.9–81.7% in P. leucocorona . Thus, parasitism was a major mortality factor in the present Phyllonorycter species. The parasitoid composition was distinctly different between the two host species, although most parasitoids were able to parasitize both leaf miner species. The analysis based on the quantitative parasitoid overlap revealed that the present parasitoids could mediate interactions between the present leaf miner species, but their effects would be weak. This is attributable to parasitoid's preferential uses of either of the leaf miners as a host.     

Exploitative competition and coexistence in a parasitoid assemblage

Most insect populations are exploited by a complex of different parasitoid species, providing ample opportunities for competitive interactions among the latter. Despite this, resource-mediated competition (i.e., exploitative competition) among insect parasitoids remains poorly documented in natural systems. Here we propose a novel way to infer the presence of competitive interactions from covariance patterns in parasitism levels, and illustrate the use of this approach on a relatively well-defined and simple host–parasitoid system. The parasitism levels caused by three parasitoid species on a shared host showed a highly consistent negative covariance among samples. With the levels of parasitism by one species increasing, the levels of parasitism attributable to the two others decreased. Importantly, negative covariance between parasitism levels by different species appeared at high abundance, but not at low abundance of the phenologically earlier parasitoid species. This as well as several other lines of evidence indicates the importance of competitive interactions in this system. Feeding biology and phenology of the parasitoids suggest that competition in this parasitoid assemblage is primarily resource-mediated rather than occurring through direct interference. The species attacking earlier stages of the host are competitively superior to those attacking their host later in the season. Better dispersal ability and use of alternative host species by the inferior species could contribute to the coexistence of these competing parasitoids.     

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.     

Comparative food web structure of larval macrolepidoptera and their parasitoids on two riparian tree species

Single species or groups of species can be subjected to differing levels of parasitism on different plants. Previous studies have reported that parasitism of larval macrolepidoptera in an assemblage on box elder (Acer negundo L.) was significantly greater than on black willow [Salix nigra (Marsh)]. In this study, quantitative food webs, parasitoid overlap diagrams and other food web attributes were used to identify and describe direct and indirect interactions, and to compare assemblages on each tree species. These comparisons helped identify possible mechanisms explaining the differential parasitism observed. Although links among numerically dominant species in each assemblage were not strong, links between numerically dominant and subdominant species were strong. That is, numerically dominant and subdominant species interacted via shared parasitoids. The degree of parasitoid sharing by numerically dominant and subdominant species differed in each tree. There was less sharing of parasitoids on black willow than on box elder. Further, on box elder, the majority of parasitoids affecting numerically subdominant species originated from numerically dominant species, unlike in willow. These results lead to a working hypothesis—the source/nursery hypothesis—that proposes that community-wide levels of parasitism are highest in circumstances in which numerically subdominant species share parasitoid species in common with numerically dominant species, and most parasitoids attacking subdominant species originate from numerically dominant species. Thus, differences in degree of sharing and the types of herbivores sharing parasitoids may explain differential parasitism. Further, the source/nursery hypothesis may explain why the vast majority of species in most assemblages are numerically subdominant. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Variations in parasitism in sympatric populations of three invasive leaf miners

Abstract:  Parasitism was investigated in sympatric populations of three invasive gracillariid leaf miners in Europe, Cameraria ohridella , Phyllonorycter robiniella and Phyllonorycter platani to test the hypotheses that C. ohridella is less heavily parasitized by native parasitoids and attacked by fewer species than the two other invasive species. In all regions investigated, C. ohridella showed a lower parasitism rate, and its parasitoid complex was poorer in species than those of either Phyllonorycter spp. Comparisons were made between sympatric populations of C. ohridella on its main host tree, Aesculus hippocastanum , and an occasional host, Acer pseudoplatanus . Parasitism rates were similarly low and composed of the same parasitoid species on both trees. In contrast, a sympatric population of Phyllonorycter geniculella , a native species mining A. pseudoplatanus , was heavily parasitized by a totally different parasitoid complex. These results suggest that the low parasitism in C. ohridella by native polyphagous leaf miner parasitoids is due neither to its host tree, nor to a problem of synchronization between the phenology of the pest and that of its parasitoids. Instead, it probably results from the inability of the native parasitoids to locate, attack, or develop on a new host that does not have any native congener in Europe.     

Effects of patch scale on density-dependence and species-dependence in two host-parasitoid systems

Summary Data from two host-parasitoid communities were analyzed to ascertain whether patch scale affected the kinds of correlations existing between 1) spatial differences in host density and the intensity of parasitism (density-dependence) and 2) number of species of parasitoids and the intensity of parasitism (species-dependence). We concluded that parasitization rates are usually independent of both host density and number of parasitoid species present regardless of patch scale. Therefore, the responses of parasitoids to host density and the addition of parasitoid species to a community are equally unpredictable in outcome.     

Parasitoid complex of the bird cherry ermine moth Yponomeuta evonymellus in Korea

The parasitoid complex of Yponomeuta evonymellus L. (Lepidoptera: Yponomeutidae), the bird cherry ermine moth (BCEM), was sought in South Korea with the goal of identifying its potential biological controls. Thirteen primary and two secondary parasitoids were found. Diadegma armillatum (Grav.), Herpestomus brunnicornis Grav. (Icheumonidae), and Zenillia dolosa (Meigen) (Tachinidae) were the most important parasitoids causing 3.5%, 7.1%, and 7.7% of the combined parasitism of the host larvae and pupae, respectively. The composition of parasitoid species was more diverse in larvae than in pupae; 10 species were reared from larvae, compared to six from pupae. The parasitoid complex contributed to the relatively low mortality levels of Yponomeuta evonymellus with the combined total rate of parasitism of 29.6% for the host larvae and pupae. This level is below that found in some European populations (50%) and is not greater than the larval rate of parasitism (31%) found in the congeneric apple ermine moth in Korea. This low rate of parasitism is partly attributed to the parasitism by Ageniaspis fuscicollis (1%) detected in Yponomeuta evonymellus, which is similar to that detected in Yponomeuta evonymellus in European reports. This is the first report of the parasitoid complex attacking the BCEM in Korea.     

Coevolution of Contrary Choices in Host-Parasitoid Systems

We investigate patch selection strategies of hosts and parasitoids in heterogeneous environments. Previous theoretical work showed that when host traits vary among patches, coevolved populations of hosts and parasitoids make congruent choices (i.e., hosts and parasitoids preferentially select the same patches) and exhibit direct density dependence in the distribution of percent parasitism. However, host-parasitoid systems in the field show a range of patterns in percent parasitism, while behavioral studies indicate that hosts and parasitoids can exhibit contrary choices (i.e., hosts avoid patches favored by the parasitoid). We extend previous theory by permitting life-history traits of the parasitoid as well as the host to vary among patches. Our analysis implies that in coevolutionarily stable populations, hosts preferentially select patches that intrinsically support higher host equilibrium numbers (i.e., the equilibrium number achieved by hosts when both populations are confined to a single patch) and that parasitoids preferentially select patches that intrinsically support higher parasitoid equilibrium numbers (i.e., the equilibrium number achieved by the parasitoids when both populations are confined to a patch). Using this result, we show how variation in life-history traits among patches leads to contrary or congruent choices or leads to direct density dependence, inverse density dependence, or density independence in the distribution of percent parasitism. In addition, we determine when populations playing the coevolutionarily stable strategies are ecologically stable. Our analysis shows that heterogeneous environments containing patches where the intrinsic rate of growth of the host and the survivorship rate of the parasitoid are low result in the coevolved populations exhibiting contrary choices and, as a result, promote ecological stability.     

Spatial variability of hosts,parasitoids and their interactions across a homogeneous landscape

Species assemblages and their interactions vary through space, generating diversity patterns at different spatial scales. Here, we study the local‐scale spatial variation of a cavity‐nesting bee and wasp community (hosts), their nest associates (parasitoids), and the resulting antagonistic network over a continuous and homogeneous habitat. To obtain bee/wasp nests, we placed trap‐nests at 25 sites over a 32 km² area. We obtained 1,541 nests (4,954 cells) belonging to 40 host species and containing 27 parasitoid species. The most abundant host species tended to have higher parasitism rate. Community composition dissimilarity was relatively high for both hosts and parasitoids, and the main component of this variability was species turnover, with a very minor contribution of ordered species loss (nestedness). That is, local species richness tended to be similar across the study area and community composition tended to differ between sites. Interestingly, the spatial matching between host and parasitoid composition was low. Host β‐diversity was weakly (positively) but significantly related to geographic distance. On the other hand, parasitoid and host‐parasitoid interaction β‐diversities were not significantly related to geographic distance. Interaction β‐diversity was even higher than host and parasitoid β‐diversity, and mostly due to species turnover. Interaction rewiring between plots and between local webs and the regional metaweb was very low. In sum, species composition was rather idiosyncratic to each site causing a relevant mismatch between hosts and parasitoid composition. However, pairs of host and parasitoid species tended to interact similarly wherever they co‐occurred. Our results additionally show that interaction β‐diversity is better explained by parasitoid than by host β‐diversity. We discuss the importance of identifying the sources of variation to understand the drivers of the observed heterogeneity.     

Seasonal patterns of parasitism and differential susceptibility among species in macrolepidopteran assemblages on Salix nigra (Marsh) and Acer negundo L.

Abstract 1. Previous research has demonstrated that parasitism of larval macrolepidoptera on Acer negundo (box elder) is greater than that of larvae on Salix nigra. 2. In this study, percentage larval parasitism of species on box elder and black willow was calculated for distinct portions of the season, to determine if the higher levels of parasitism on box elder resulted from greater parasitism during a particular portion of the season. 3. Larval parasitism was higher on box elder regardless of the portion of the season; however, the seasonal pattern of parasitism differed for each tree species, i.e. late-season box elder parasitism increased and late-season black willow parasitism decreased relative to early- and mid-season parasitism. 4. The degree to which higher levels of parasitism were associated with host and parasitoid traits such as average larval abundance, number of species, type of host, and parasitoid species load of macrolepidoptera, as well as average number of species of parasitoids during each portion of the season was determined. 5. In addition, the possibility that differences in the pattern of parasitism on box elder and black willow were caused by the presence of a greater number of numerically dominant parasitoid species in late-season box elder was investigated. 6. None of the variables, other than type of host species, were associated with higher levels of parasitism in late-season box elder. 7. Late-season, single-tree species on box elder (i.e. species that occurred only on box elder) were more heavily parasitised, compared with dual-tree species. This difference was not observed earlier in the season nor on black willow. 8. Further, single-tree species on late-season box elder included three numerically dominant species that suffered significantly greater larval parasitism than any other type of species on either of the two trees. 9. This study supported previous predictions, that suggested the importance of larval coloration: there was a higher proportion of green larvae among the most highly parasitised host species, i.e. single-tree, numerically dominant species.     

Development of the parasitoid,Cotesia rubecula (Hymenoptera: Braconidae) in Pieris rapae and Pieris brassicae (Lepidoptera: Pieridae): evidence for host regulation

Several recent models examining the developmental strategies of parasitoids attacking hosts which continue feeding and growing after parasitism (=koinobiont parasitoids) assume that host quality is a non-linear function of host size at oviposition. We tested this assumption by comparing the growth and development of males of the solitary koinobiont endoparasitoid, Cotesia rubecula, in first (L1) to third (L3) larval instars of its preferred host, Pieris rapae and in a less preferred host, Pieris brassicae. Beginning 3 days after parasitism, hosts were dissected daily, and both host and parasitoid dry mass was determined. Using data on parasitoid dry mass, we measured the mean relative growth rate of C. rubecula, and compared the trajectories of larval growth of the parasitoid during the larval and pupal stages using non-linear equations. Parasitoids generally survived better, completed development faster, and grew larger in earlier than in later instars of both host species, and adult wasps emerging from P. rapae were significantly larger than wasps emerging from all corresponding instars of P. brassicae. During their early larval stages, parasitoids grew most slowly in L1 P. rapae, whereas in all other host classes of both host species growth to pupation proceeded fairly uniformly. The growth of both host species was markedly reduced after parasitism compared with controls, with the development of P. brassicae arrested at an earlier stage, and at a smaller body mass, than P. rapae. Our results suggest that C. rubecula regulates certain biochemical processes more effectively in P. rapae than in P. brassicae, in accordance with its own nutritional and physiological requirements. Furthermore, we propose that, for parasitoids such as C. rubecula, which do not consume all host tissues prior to pupation, that parasitoid size and host quality may vary independently of host size at oviposition and at larval parasitoid egression.