High nymphal host density and mortality negatively impact parasitoid complex during an insect herbivore outbreak

Insect herbivore outbreaks frequently occur and this may be due to factors that restrict top-down control by parasitoids, for example, host-parasitoid asynchrony, hyperparasitization, resource limitation and climate. Few studies have examined hostparasitoid density relationships during an in sect herbivore outbreak in a n atural ecosystem with diverse parasitoids. We studied parasitization patterns of Cardiaspina psyllids during an outbreak in a Eucalyptus woodland. First, we established the trophic roles of the parasitoids through a species-specific multiplex PCR approach on mummies from which parasitoids emerged. Then, we assessed host-parasitoid density relationships across three spatial scales (leaf, tree and site) over one yeas We detected four endoparasitoid species of the family Encyrtidae (Hymenoptera);two primary parasitoid and one heteronomous hyperparasitoid Psyllaephagus species (the latter with female development as a primary parasitoid and male development as a hyperparasitoid), and the hyperparasitoid Coccidoctonuspsyllae. Parasitoid development was host-synchronized, although synchrony between sites appeared constrained during winter (due to temperature differences). Parasitization was predominantly driven by one primary parasitoid species and was mostly inversely host-density dependent across the spatial scales. Hyperparasitization by C. psyllae was psyllid-density dependent at the site scale, however, this only impacted the rarer primary parasitoid. High larval parasitoid mortality due to density-dependent nymphal psyllid mortality (a consequence of resource limitation) compounded by a summer heat wave was incorporated in the assessment and resulted in density independence of host-parasitoid relationships. As such, high larval parasitoid mortality during insect herbivore outbreaks may contribute to the absence of host density-dependent parasitization during outbreak events.     

Species richness and parasitism in an assemblage of parasitoids attacking maize stem borers in coastal Kenya

Abstract. 1. Parasitoids were reared from four species of lepidopteran stem borer collected in maize in southern coastal Kenya from 1992 to 1999. The stem borers included three native species, Sesamia calamistis Hampson, Busseola fusca Fuller, and Chilo orichalcociliellus (Strand), and one exotic borer, Chilo partellus (Swinhoe). A total of 174 663 caterpillars was collected, of which 12 645 were parasitised.
2. Twenty-six primary parasitoid species were reared from the exotic borer, C. partellus , indicating a rapid accumulation of native parasitoids on the alien borer.
3. The three most abundant parasitoids were the larval parasitoids Cotesia sesamiae Cameron, Cotesia flavipes (Cameron), and the pupal parasitoid Pediobius furvus Gahan. The pupal parasitoid Dentichasmias busseolae Heinrich and the larval parasitoid Goniozus indicus Ashmead were also common. All used an ingress-and-sting method of attack.
4. Cotesia flavipes , introduced into Kenya in 1993, was found in all seasons from 1997 onwards, and has become the most abundant stem borer larval parasitoid in the area. A native congener, Cotesia sesamiae , appeared in all seasons from 1992 to 1999. Together, these two parasitoids accounted for 83.3% of the parasitised borers.
5. Thirty parasitoid species were recovered in Kilifi district, 27 in Kwale, and 15 in Taita Taveta. Parasitism was much greater in Taita Taveta district than in Kilifi or Kwale districts.     

Environmental thermal levels affect the phenological relationships between the chestnut gall wasp and its parasitoids

Studies of thermal level‐related asynchrony in a host–parasitoid relationship are necessary to understand the effects of climate change on new host–parasitoid interactions. In the Asian chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae) and its Chalcidoidea parasitoids, phenological synchrony is assumed to be weather‐dependent in a new area of expansion. To evaluate the effects of environmental thermal regimes on the host, a phenology model for different cynipid stages (larvae, pupae, adults, and adult emergence) and a host–parasitoid phenological estimator are developed in three chestnut fields during two successive growth seasons and subsequently validated in areas with chestnut fields at two different altitudes. Comparisons of the timings of the juvenile and adult stages with those of the parasitoid complex demonstrate that the shortest period of occurrence for cynipids within galls has negative effects on the host–parasitoid relationships at higher temperature levels, thereby increasing phenological asynchrony for some parasitoids species. Reducing the development time of pupae and adults decreases the likelihood of success for some parasitoid species at higher temperature levels. We also record the extension of the gall wasp development time (approximately 15 days) at higher altitudes (linked to a lower mean temperature of approximately 1.5 °C). These results highlight how parasitization on the new hosts is dependent on the host phenology and, in the present study, is limited by the short duration of the presence of the host in galls, which could explain the considerable differences in cynipid gall wasp parasitization recorded at different altimeters.     

A survey of hymenopteran parasitoids of forest macrolepidoptera in the central Appalachians

In 1995 and 1996, we conducted a study of the hymenopteran parasitoids of macrolepidopteran larvae in the George Washington National Forest (GWNF), Augusta County, Virginia, and the Monongahela National Forest (MNF), Pocahontas County, West Virginia. Macrolepidopteran larvae were collected from canopy foliage and from under canvas bands placed around tree boles. A total of 115 macrolepidopteran species and 5,235 individual larvae were reared. Forty-two percent (2,221) of the larvae were gypsy moth, Lymantria dispar (L.) (Lymantriidae). A total of 43 primary and secondary (hyperparasitoid) hymenopteran parasitoid species were reared from 46 macrolepidopteran species. Hymenopteran families represented included Ichneumonidae (23 species), Braconidae (19), Eulophidae (6), Perilampidae (1), and Trigonalidae (1). We reared 41 and 28 parasitoid species from the GWNF and the MNF, respectively, with 19 species reared from both forests. Many parasitoid species were collected infrequently, suggesting that they are relatively rare on the sampled hosts. The introduced species Cotesia melanoscela (Ratzeburg) (Braconidae), and Euplectrus bicolor (Swederus) (Eulophidae) were among the most commonly reared parasitoids, the latter reared from native hosts. The four most commonly reared native parasitoids were Meteorus hyphantriae, Riley (Braconidae), Microplitis near hyphantriae (Ashmead) (Braconidae), Aleiodes preclarus Marsh & Shaw, and Euplectrus maculiventris (Westwood) (Eulophidae). A total of 53 new hymenopteran parasitoid-macrolepidopteran host records were documented. Results from this study will be used to evaluate long-term treatment effects of regional applications of Bacillus thuringiensis kurstaki, and the gypsy moth fungus Entomophaga maimaiga Humber, Shimazu & Soper on hymenopteran parasitoids of macrolepidopteran larvae.     

Invasion and Displacement of Experimental Populations of a Conventional Parasitoid by a Heteronomous Hyperparasitoid

Aphelinid parasitoids have an outstanding record of success in programmes of classical biocontrol against whiteflies and scale insects. Heteronomous hyperparasitoids are aphelinids in which the sexes develop on or in different hosts. The female always develops as a primary endoparasitoid of Homoptera. The male develops as a secondary parasitoid hyperparasitoid of his own or another species of homopteran endoparasitoid. Caged experiments were performed with the cabbage whitefly, Aleyrodes proletella, to examine the invasion of a population of a conventional parasitoid, Encarsia inaron both sexes primary endoparasitoids by a heteronomous hyperparasitoid, E. tricolor. In all cages the heteronomous hyperparasitoid successfully invaded an established population of the conventional parasitoid and the conventional species population declined to very low levels within 8 weeks of the introduction of the heteronomous hyperparasitoid. The patterns of invasion were different in each cage. In two cages, high levels of male production by E. tricolor were observed, indicating that hyperparasitism of the conventional species was probably an important factor in causing the decline in the E. inaron population. In a reciprocal experiment in which E. inaron was introduced to an established population of E. tricolor the conventional species failed to invade or persist. A survey of published references to complexes of parasitoids containing a heteronomous hyperparasitoid and one or more conventional species indicated that, in the majority of cases, the heteronomous hyperparasitoid was the most important species in the complex. There are clear implications for the use of these parasitoids in programmes of classical biocontrol. This is because high competitive ability against other parasitoids is not necessarily a good indicator of the ability of a species to maintain high levels of pest control, especially when hyperparasitic behaviour is involved.     

Can hyperparasitoids cause large‐scale outbreaks of insect herbivores?

Synchronous population fluctuations occur in many species and have large economic impacts, but remain poorly understood. Dispersal, climate and natural enemies have been hypothesized to cause synchronous population fluctuations across large areas. For example, insect herbivores cause extensive forest defoliation and have many natural enemies, such as parasitoids, that may cause landscape‐scale changes in density. Between outbreaks, parasitoid‐caused mortality of hosts/herbivores is high, but it drops substantially during outbreak episodes. Because of their essential role in regulating herbivore populations, we need to include parasitoids in spatial modelling approaches to more effectively manage insect defoliation. However, classic host‐parasitoid population models predict parasitoid density, and parasitoid density is difficult to relate to host‐level observations of parasitoid‐caused mortality. We constructed a novel model to study how parasitoids affect insect outbreaks at the landscape scale. The model represents metacommunity dynamics, in which herbivore regulation, colonisation and extinction are driven by interactions with the forest, primary parasitoids and hyperparasitoids. The model suggests that parasitoid spatial dynamics can produce landscape‐scale outbreaks. Our results propose the testable prediction that hyperparasitoid prevalence should increase just before the onset of an outbreak because of hyperparasitoid overexploitation. If verified empirically, hyperparasitoid distribution could provide a biotic indicator that an outbreak will occur.     

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA-based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species-specific parasitoid-hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.     

Sequential rapid adaptation of indigenous parasitoid wasps to the invasive butterfly Pieris brassicae

The introduction of a new species can change the characteristics of other species within a community. These changes may affect discontiguous trophic levels via adjacent trophic levels. The invasion of an exotic host species may provide the opportunity to observe the dynamics of changing interspecific interactions among parasitoids belonging to different trophic levels. The exotic large white butterfly Pieris brassicae invaded Hokkaido Island, Japan, and quickly spread throughout the island. Prior to the invasion, the small white butterfly P. rapae was the host of the primary parasitoid Cotesia glomerata, on which both the larval hyperparasitoid Baryscapus galactopus and the pupal hyperparasitoid Trichomalopsis apanteroctena depended. At the time of the invasion, C. glomerata generally laid eggs exclusively in P. rapae. During the five years following the invasion, however, the clutch size of C. glomerata in P. rapae gradually decreased, whereas the clutch size in P. brassicae increased. The field results corresponded well with laboratory experiments showing an increase in the rate of parasitism in P. brassicae. The host expansion of C. glomerata provided the two hyperparasitoids with an opportunity to choose between alternative hosts, that is, C. glomerata within P. brassicae and C. glomerata within P. rapae. Indeed, the pupal hyperparasitoid T. apanteroctena shifted its preference gradually to C. glomerata in P. brassicae, whereas the larval hyperparasitoid B. galactopus maintained a preference for C. glomerata in P. rapae. These changes in host preference may result from differential suitability of the two host types. The larval hyperparasitoid preferred C. glomerata within P. rapae to C. glomerata within P. brassicae, presumably because P. brassicae larvae attacked aggressively, thereby hindering the parasitization, whereas the pupal hyperparasitoid could take advantage of the competition-free resource by shifting its host preference. Consequently, the invasion of P. brassicae has changed the host use of the primary parasitoid C. glomerata and the pupal hyperparasitoid T. apanteroctena within a very short time.     

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.     

Spatial and temporal variation in the parasitoid assemblage of an exophytic polyphagous caterpillar

Abstract 1. Over 3400 larvae of the polyphagous ground dwelling arctiid Grammia geneura were sampled and reared over seven generations in order to characterise its parasitoid assemblage and examine how and why this assemblage varies over time and space at a variety of scales.
2. The total parasitoid assemblage of 14 species was dominated both in diversity and frequency by relatively polyphagous tachinid flies.
3. Both the composition of the parasitoid assemblage and frequency of parasitism varied strikingly among and within sampling sites, seasons, and years.
4. Overall rates of parasitism increased consistently over the duration of caterpillar development.
5. Within sampling sites, parasitism rates were non-random with respect to habitat structure and caterpillar behaviour for the most abundant parasitoid species.
6. The large variability in parasitoid assemblage structure over space and time in this system may be a function of local host population abundance, habitat-specific parasitism, and indirect interactions between G. geneura and other Macrolepidoptera through shared oligophagous and polyphagous parasitoids.     

An exotic parasitoid provides an invasional lifeline for native parasitoids

The introduction of an exotic species may alter food webs within the ecosystem and significantly affect the biodiversity of indigenous species at different trophic levels. It has been postulated that recent introduction of the brown marmorated stinkbug (Halyomorpha halys (Stål)) represents an evolutionary trap for native parasitoids, as they accept H. halys egg masses as a host but produce no viable progeny. Interspecific interactions between European egg parasitoid, Trissolcus cultratus (Mayr), and an Asian parasitoid, Trissolcus japonicus (Ashmead), were assessed by providing egg masses to T. cultratus at various time intervals following the initial parasitization by T. japonicus. The suitability of the host for the parasitoid development was re‐assessed by providing T. cultratus with fresh and frozen egg masses of various ages. The likelihood of T. cultratus being able to attack previously parasitized egg masses was determined by assessing the duration of egg mass guarding behavior by T. japonicus following parasitization. The results of experiments examining the interspecific interactions between a native European egg parasitoid, T. cultratus, and an Asian parasitoid, T. japonicus (a candidate for the biological control of H. halys), showed that the native species can act as facultative hyperparasitoid of the exotic one. Although this is only possible during certain stages of T. japonicus development, the presence of the introduced parasitoid may reduce the impact of the evolutionary trap for indigenous parasitoid species. There is a possibility that the occurrence of facultative hyperparasitism between scelionid parasitoids associated with stinkbugs is common. This resulting intraguild predation could promote conservation and stabilization of natural communities by impacting the diversity and population dynamics of native stinkbugs and their parasitoids (e.g., by allowing native parasitoids to avoid wasting reproductive effort on unsuitable hosts), or reduce success of biological control programs (e.g., by reducing the population size of the exotic parasitoids).     

Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae)

The role of winter diapause in two aphid parasitoid species, Aphidius ervi Haliday and Aphidius rhopalosiphi DeStefani-Peres (Hymenoptera: Braconidae: Aphidiinae), in host synchronization and the induction of cold hardiness was investigated. Parasitoids were reared during three successive generations on Sitobion avenae Fabricius, at 15 degrees C under a photoperiod of 9 h light 15 h dark. Although these conditions are known to be strongly diapause inducing, neither parasitoids showed an incidence of diapause above 65% over the three generations; the rest of the population underwent quiescence. In both parasitoid species, diapausing mummies exhibited greater cold hardiness than non-diapausing mummies, resulting in significantly lower supercooling points (SCP) and in a higher survival rate during long-term exposures at 0 and -10 degrees C. The induction of increased cold hardiness in parasitoids was thus associated with the diapause state. SCPs of third instar larvae of S. avenae were similar to those of non-diapausing mummies of both parasitoid species, but significantly higher than those of diapausing mummies. The effect of winter climate on the stability of the host-parasitoid interaction is discussed.     

Effects of dietary nicotine on the development of an insect herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels

Abstract.  1. Allelochemicals in herbivore diet are known to affect the development of higher trophic levels, such as parasitoids and predators.
2. This study examines how differing levels of nicotine affects the development of a herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels. Separate cohorts of the herbivore, Manduca sexta , were fed on artificial diets containing 0.0, 0.1, and 0.5% wet weights of nicotine. Some of the larvae in each cohort were separately parasitised in the first (L1) and third (L3) instars by the gregarious endoparasitoid, Cotesia congregata . Newly emerged parasitoid cocoons were, in turn, parasitised by the hyperparasitoid, Lysibia nana .
3. Pupal mass in M . sexta was negatively correlated with nicotine concentrations in the artificial diet, although larval development time was unaffected.
4. Hyperparasitoid survival was highest when there were low levels of nicotine in the diet of M . sexta . Cocoon mass in C . congregata and adult mass in L . nana were mostly affected by nicotine levels in host diet when L1 M. sexta larvae were parasitised. The effects were slightly stronger on L . nana than on C . congregata , indicating the presence of both qualitative and quantitative effects of nicotine concentration on both species.
5. The results suggest that allelochemicals in herbivore diet can have both direct and indirect effects on the performance of higher trophic levels. However, in multitrophic interactions these effects can vary with the stage of the herbivore attacked by the primary parasitoid, as well as with the strategy employed by the herbivore to deal with plant phytotoxins.     

Increased Parasitization of Aphids on Trap Plants Alongside Vials Releasing Synthetic Aphid Sex Pheromone and Effective Range of the Pheromone

Aphid-infested cereal trap plants were used to detect the effects of aphid sex pheromone components on aphid parasitoid activity in arable field margins. The presence of aphid sex pheromones significantly increased parasitization levels by aphid parasitoids on the plants. By placing plants alongside and at varying distances away from a pheromone-releasing vial, the technique was used to measure the distance over which a point source of aphid sex pheromone could increase parasitization levels. Pheromone-releasing vials significantly increased parasitization by the generalist parasitoid Praon volucre on plants adjacent to vials and on plants placed 20 cm away. When the distance between pheromone-releasing vials and aphid-infested plants was increased to 1 m, parasitization by P. volucre was increased only on the plant adjacent to the vial, whereas parasitization by the specialist parasitoid Aphidius rhopalosiphi was also increased on plants placed 1 m away. This indicates a possible difference between the parasitoids in their foraging behaviour in response to semiochemical cues during host selection. When the experiment was repeated with some trap plants placed 3 m away from the pheromone-releasing vial, parasitization was again concentrated on plants directly alongside the vial, but only P. volucre appeared to be active in the field at the time of this experiment, so the effect on A. rhopalosiphi could not be assessed. The results are encouraging for the prospects of using aphid sex pheromones to manipulate parasitoids in order to improve aphid population control.     

Changes in function and temporal variation in a guild of gall‐parasitoids across a temperature gradient in Australian subtropical rainforest

Parasitoids play an important role in ecosystem functioning through their influence on herbivorous insect populations. Theoretical and experimental evidence suggest that increased species richness can enhance and stabilize ecosystem function. It is important to understand how richness‐driven functional relationships change across environmental gradients. We investigated how temperature affected the relationship between parasitoid richness and parasitism rate in a guild of gall‐parasitoids along an elevational gradient. We collected galls at 15 sites along five elevational gradients (between 762 m and 1145 m asl) on six occasions over a year. A total of 1902 insects, including 1593 parasitoids, were reared from 12 402 galls. Parasitism rate increased significantly with temperature on all sampling occasions, except December and February. We found a significant, positive richness–parasitism relationship. This relationship, however, was weaker at higher elevations which may be linked to decreased functional efficiency of parasitoids at lower temperatures. Temporal variability in parasitism rate and parasitoid richness were significantly related, regardless of temperature. A stable functional guild of this kind may provide a more reliable ecosystem service under environmental changes.     

The response of aphid secondary parasitoids to different patch densities of their host

Aphids are attacked by a large guild of natural enemies including many primary parasitoids which mummify their hosts. These mummies are themselves attacked by a guild of mummy parasitoids which are potentially important in regulating primary parasitoids at densities below which they can exert biological control. The response of mummy parasitoids to mummy densities was investigated in an experiment in which mummy densities of the pea aphid (Acyrthosiphon pisum) attacked by the parasitoid Aphidius ervi were manipulated across host plant patches. Overall, the risk of parasitism was density independent, though with very high inter-patch variability which may allow probabilistic refuges from secondary parasitism. Six species of four genera of mummy parasitoids were recorded. Of the responses of the individual genera, Coruna were reared most frequently from patches of high host density while amongst patches from which Syrphophagus was reared parasitism was inversely density dependent.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Cascading effects of host size and host plant species on parasitoid resource allocation

1. The bottom‐up factors that determine parasitoid host use are an important area of research in insect ecology. Host size is likely to be a primary cue for foraging parasitoids due to its potential influence on offspring development time, the risk of multiparasitism, and host immunocompetence. Host size is mediated in part by host‐plant traits that influence herbivore growth and potentially affect a herbivore's quality as a host for parasitoids. 2. Here, we tested how caterpillar host size and host plant species influence adult fly parasitoid size and whether host size influences wasp parasitoid sex allocation. We measured the hind tibia lengths and determined the sex of wasp and fly parasitoids reared from 11 common host species of polyphagous caterpillars (Limacodidae) that were in turn reared on foliage of seven different host plant species. 3. We also tested how host caterpillar species, host caterpillar size, and host and parasitoid phenology affect how the parasitoid community partitions host resources. We found evidence that parasitoids primarily partition their shared hosts based on size, but not by host species or phenology. One index of specialisation (d′) supports our observation that these parasitoids are quite generalised within the Limacodidae. In general, wasps were reared from caterpillars collected in early instars, while flies were reared from caterpillars collected in late instars. Furthermore, for at least one species of solitary wasp, host size influenced sex allocation of offspring by ovipositing females. 4. Host‐plant quality indirectly affected the size attained by a tachinid fly parasitoid through its direct effects on the size and performance of the caterpillar host. The host plants that resulted in the highest caterpillar host performance in the absence of enemies also yielded the largest parasitoid flies, which suggests that host plant quality can cascade up to influence the third trophic level.     

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.     

Four‐level interactions: herbivore use of ferns and subsequent parasitoid–hyperparasitoid performance

Abstract 1. Variables affecting species at the ends of trophic chains may modify the success of members with which they do not directly interact. The majority of such examples involve three trophic levels, but hyperparasitoids provide an excellent opportunity to examine four‐level relationships. 2. The gregarious hyperparasitoid Aprostocetus sp. (Hymenoptera: Eulophidae) commonly attacks the primary parasitoid Alabagrus texanus (Hymenoptera: Braconidae), by far the commonest parasitoid of the moth Herpetogramma theseusalis (Lepidoptera: Crambidae). 3. Larvae of this moth feed on ferns of two families, sensitive fern Onoclea sensibilis (Dryopteridaceae) and marsh fern Thelypteris palustris (Thelypteridaceae), in the study area, an old field in Maine, U.S.A. 4. I test the hypotheses that the ferns indirectly affect the reproductive success of the hyperparasitoids and that the ferns produce similar effects at intermediate links. 5. The moths experienced similar success on the two ferns, and the primary parasitoid performed similarly on moths reared from both ferns. The hyperparasitoid parasitized similar proportions of the primary parasitoid from moths that fed on sensitive fern and marsh fern. 6. However, hyperparasitoid broods on primary parasitoids from moths feeding on marsh fern contained approximately one‐third more offspring, whose individuals were significantly larger than those from sensitive fern, even though their hosts’ sizes did not differ significantly. 7. An indirect effect, related to the primary producers, thus strongly affected Trophic Level 4 in the absence of a significant effect at intermediate levels. To the best of my knowledge, this relationship has not been previously reported in a multi‐year or field‐based study of a natural system.