Intrinsic competition between primary hyperparasitoids of the solitary endoparasitoid Cotesia rubecula

1. In nature, competitive interactions occur when different species exploit similar niches. Parasitic wasps (parasitoids) often have narrow host ranges and need to cope with competitors that use the same host species for development of their offspring. When larvae of different parasitoid species develop in the same host, this leads to intrinsic and often contest competition. Thus far, most studies on intrinsic competition have focused on primary parasitoids. However, competition among primary hyperparasitoids, parasitic wasps that use primary parasitoids as a host, has been little studied. 2. This study investigated intrinsic competition between two primary hyperparasitoids, the gregarious Baryscapus galactopus and the solitary Mesochorus gemellus, which lay their eggs in primary parasitoid larvae of Cotesia rubecula, while those in turn are developing inside their herbivore host, Pieris rapae. The aims were to identify: (i) which hyperparasitoid is the superior competitor; and (ii) whether oviposition sequence affects the outcome of intrinsic competition. 3. The results show that B. galactopus won 70% of contests when the two hyperparasitoids parasitised the host at the same time, and 90% when B. galactopus oviposited first. When M. gemellus had a 48 h head start, the two hyperparasitoids had an equal chance to win the competition. This suggests that B. galactopus is an intrinsically superior competitor to M. gemellus. Moreover, the outcome of competition is affected by time lags in oviposition events. 4. In contrast to what has been reported for primary parasitoids, we found that a gregarious hyperparasitoid species had a competitive advantage over a solitary species.     

Colonization and hyperparasitism ofCotesia rubecula (Hym.: Braconidae), a newly introduced parasite ofPieris rapae,in Virginia

A Yugoslavian strain ofCotesia rubecula (Marshall) (Hymenoptera: Braconidae) was released in spring broccoli for control of the imported cabbageworm,Pieris rapae (L.), in Montgomery Co., Virginia, in 1987.C. rubecula reproduced and parasitized imported cabbageworm larvae in fall broccoli in 1987. It was found in moderate numbers in the summer and fall crops in 1988, and by fall had dispersed 0.8 km from the original release site. However, noC. rubecula were detected in our broccoli plots in Montgomery Country in 1989 or 1990. The hymenopteran hyperparasitesIsdromas lycaenae (Walker)(Ichneumonidae), Spilochalcis torvina (Cresson) (Chalcididae), andTetrastichus galactopus (Ratzeburg) (Eulophidae) were found attackingC. rubecula. Hyperparasites emerged from 31.8% and 41.1% of theC. rubecula cocoons in 1987 and 1988, respectively.T. galactopus was the most numerous hyperparasite in 1987, butS. torvina was dominant in 1988. Hyperparasite activity was low during early spring, but increased in July in both years. By August 1988, only hyperparasites emerged from theC. rubecula cocoons collected in the field. In spite ofC. rubecula's success in overwintering, hyperparasites, especiallyS. torvina, may be a limiting factor in the establishment ofC. rubecula in southwestern Virginia.      

The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species)

The main objective of this study was to determine the extent to which host acceptance behaviour as related to host species, age, and defensive behaviour might explain the differences in host use that exist between two congeneric and sympatric species of parasitic wasps. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). Cotesia species differed in their responses to host species (P. brassicae (L.), P. napi (L.) and P. rapae) and developmental stage (early and late 1st, 2nd and 3rd instars). In no-choice tests, host acceptance by C. rubecula was higher for p. rapae and females did not distinguish among the 6 host ages. In contrast, when foraging for P. brassicae and P. napi, C. rubecula females more readily attacked early first instar. Cotesia glomerata showed a higher degree of behavioural plasticity towards acceptance of Pieris host species and host age than did C. rubecula. Cotesia glomerata females parasitized the three Pieris species and showed higher acceptance of first and second instars over third instar. Oviposition success was also influenced by host defensive behaviour. The frequency and the effectiveness of defensive behaviour rose with increasing age of the host, P. brassicae being the most aggressive Pieris species. Furthermore, the mean duration of C. glomerata oviposition was significantly reduced by the defensive reactions of P. brassicae, which would likely affect parasitoid fitness as oviposition time is positively correlated to clutch size in C. glomerata. Acceptance frequencies corresponded well to field reports of Pieris-Cotesia associations and to patterns of parasitoid larval performance, suggesting that the acceptance phase might be used as a reliable indicator of Cotesia host-specificity.     

Influences of plant species on life history traits of Cotesia rubecula (Hymenoptera: Braconidae) and its host Pieris rapae (Lepidotera: Pieridae)

The relative suitability of four plants was studied for larvae of Pieris rapae L. and its parasitoid Cotesia rubecula (Marshall). For unparasitized P. rapae, pupal dry weight and egg-pupa growth rate were higher on cabbage, radish and nasturtium than on Indian hedge mustard. Larval developmental rate and size were greatest for C. rubecula when its host was feeding on nasturtium. Wasp survival was not affected by the host insect/plant combination in which the parasitoid developed. These results indicate that the plant on which host larvae feed is an important factor in development of the parasitoid.     

Oviposition pattern byCotesia ayerzai [Hym.: Braconidae] onAscia monuste [Lep.: Pieridae] under laboratory conditions

Various aspects of the parasitims of caterpillars ofAscia monuste orseis byCotesia ayerzai, were studied in laboratory choice tests. Individual ♂♂ were found to be extremely variable in ovipositional duration, as well as in the number of eggs oviposited. To simulate parasitoid dispersal, or low host density, we isolated ♂♂ for 60 min following initial exposure and compared our tests with ♂♂ which had not been isolated. No differences in (1) the number of eggs oviposited per host instar; (2) the conditional probability of host encounter; (3) host acceptance; and (4) the conditional probability of instar specific parasitism were found between these groups. Held ♂♂ did, however, reject hosts after ovipositor insertions in a higher proportion.      

Foraging for solitarily and gregariously feeding caterpillars: A comparison of two related parasitoid species (Hymenoptera: Braconidae)

In the present study we apply a comparative approach, in combination with experimentation, to study behavior of two parasitoid species that attack caterpillar hosts with different feeding strategies (gregarious or solitary). In a semifield setup, consisting of clean cabbage plants and plants infested with one of two host species, the foraging behavior of the specialistCotesia rubecula, on obligate parasitoid of solitarily feedingPieris rapae larvae, was compared to that of the generalistCotesia glomerata, a polyphagous parasitoid of several Pieridae species (mainly the gregariously feedingPieris brassicae).Cotesia glomerata displayed equal propensity to search for and parasitize larvae of both host species. AlthoughC. glomerata exhibited a relatively plastic foraging behavior in that it searched differently under different host distribution conditions, its behavior seems more adapted to search for gregariously feeding hosts. Females exhibited a clear area-restricted search pattern and were more successful in finding the gregariously feeding caterpillars.Cotesia rubecula showed a higher propensity to search forP. rapae than forP. brassicae, i.e., females left the foraging setup significantly earlier when their natural hostP. rapae was not present.C. rubecula showed a more fixed foraging behavior, which seems adapted to foraging for solitarily feeding host larvae. In a setup with onlyP. rapae larvae, the foraging strategies of the two parasitoid species were quite similar. In a choice situationC. glomerata did not show a preference for one of the host species, whileCotesia rubecula showed a clear preference for its natural host species. The latter was shown by several behavioral parameters such as the number of first landings, allocation of search time, and percentage parasitization.     

Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoidCotesia rubecula

The role of volatile stimuli in the long-range host-searching behaviour of the specialist parasitoidCotesia rubecula Marshall (Hymenoptera: Braconidae) was studied. Components from the plant-host-complex Brussels sprouts (Brassica oleracea L. var.gemmifera (DC.) Schulz. cv. ‘Titurel’)-Pieris rapae L. (Lepidoptera: Pieridae) were compared for their attractiveness in dual choice tests in a windtunnel. Stimuli from cabbage plants that were mechanically damaged or damaged byP. rapae caterpillars were more attractive to this parasitoid species than stimuli emitted by the host larvae or their faeces. Parasitoids preferred leaves from the plant-host-complex over artificially damaged leaves. Undamaged cabbage plants were the least attractive to the foraging females. These results indicate that in-flight searching behaviour ofC. rubecula is guided by plant-derived information and that for this specialist species more reliable and specific host-derived cues play a minor role at longer distances.     

Interactions between an eucoilid [Hymenoptera] and a staphylinid [Coleoptera] parasitoid of the cabbage root fly

The interaction betweenTrybliographa rapae andAleochara bilineata, 2 parasitoids of the cabbage root fly, is discussed. Larvae ofA. bilineata could not differentiate between cabbage root fly pupae containingT. rapae in its endoparasitic state and unparasitized pupae but could recognize pupae containingT. rapae once the latter had reached its ectoparasitic state. Attack byA. bilineata whileT. rapae was still in its endoparasitic state usually resulted in the staphylinid killing the eucoilid. IfT. rapae had reached the ectoparasitic state before the host pupa was attacked byA. bilineata larvae the eucoilid survived attack by the beetle larva. Multiparasitism, however, resulted in increased levels of mortality of both parasitoid populations.      

The introduction and recovery in the United States ofAnaphes diana [Hym.: Mymaridae], an egg parasite ofSitona weevils [Col.: Curculionidae]

Anaphes diana (Girault) (=Patasson lameerei Debauche), a mymarid egg parasite ofSitona spp., was introduced from Europe beginning in 1976 and is now tentatively established in the United States. Techniques are described for the separation of eggs ofSitona spp. from soil, using a series of fine-mesh sieves, water, and a saturated salt solution. Data from 9 years of sampling in an alfalfa field at Newark, Del. (>19,300 host eggs extracted), showed that the mean peak density of viable overwintering eggs ofSitona hispidulus (F.) was 14.6 per 100 cm³ of 1 cm deep surface soil. At the study site,Sitona egg densities consistently increased during the fall as a result of oviposition, peaked during January and February and decreased during the spring as a result of egg hatch. Although the incidence of parasitism byA. diana remained surprisingly low (0.29%), the fact that the species was recovered during 3 years and up to 7 years after the last release, indicates that it has colonized at the Delaware release site.      

Foraging behavior and life history of the stemborer parasitoidCotesia flavipes (hymenoptera: Braconidae)

The gregarious parasitoidCotesia flavipes (Hymenoptera: Braconidae) attacks larvae of pyralid and noctuid stemborers by entering the stemborer tunnel. The short-range foraging behavior of femaleC. flavipes was studied on stemborerinfested plants, in patches with host-related products and in artificial transparent tunnels. In addition, the longevity under specific conditions and the potential and realized fecundity of femaleC. flavipes were determined. Larval frass, caterpillar regurgitate, and holes in the stem are used in host location byC. flavipes. The response to host products byC. flavipes seems not to be host species specific. FemaleC. flavipes respond to frass from four stemborer species and one leaf feeder. No differences are found in the behavior ofC. flavipes on maize plants infested with the suitable host,Chilo partellus (Lepidoptera: Pyralidae), or the unsuitable host,Busseola fusca (Lepidoptera: Noctuidae). Attacking a stemborer larva inside the stem is risky for the parasitoid. The mortality rate of the parasitoids inside the stem is high: 30–40% of the parasitoids are killed by the spitting and biting stemborer larva.C. flavipes is relatively shortlived: without food the parasitoids die within 2 days; with food and under high-humidity conditions they die within 5–6 days.C. flavipes is proovigenic and has about 150 eggs available for oviposition. A relatively large proportion of the available egg load (20–25%) is allocated to each host, so femaleC. flavipes are egg depleted after parasitizing only five or six hosts.     

Oviposition experience on a host-infested plant affects flight and antennal searching behavior of Cotesia kariyai toward the host-plant complex

The flight response of Cotesia kariyaiWatanabe (Hymenoptera: Braconidae), a parasitoid of the polyphagous herbivore, Mythimna separataWalker (Lepidoptera: Noctuidae), to pairs of different plant species infested by M. separatalarvae was tested under a dual choice condition in the laboratory. The oviposition-inexperienced (naive) wasps showed preference in the order: corn > kidney bean > Japanese radish. Wasps that had previously oviposited on the less preferred plant in a pair were found to have shifted their preference to this plant at 2 h after oviposition. However, this shift became indistinct at 17 h after oviposition. Prior oviposition on a plant species other than those being compared also affected the preference. These data suggest that learning is involved in the wasp's flight response. Prior oviposition was also observed to have an effect on the antennal searching behavior of the wasp on corn leaves. Such behavioral plasticity may enhance the efficiency by which C. kariyaisearches for polyphagous hosts.     

Response of the wasp (<Emphasis Type="Italic">Cotesia glomerata</Emphasis>) to larvae of the large white butterfly (<Emphasis Type="Italic">Pieris brassicae</Emphasis>)

The large white butterfly (Pieris brassicae L) first invaded northernmost Japan from Siberia around 1994, and after a few years, began to expand its range. The wasp, Cotesia glomerata (L) parasitizes larvae of the small white butterfly (Pieris rapae crucivora Boisduval), a usual host in the same geographic area. Some Pieris brassicae larvae in Hokkaido have been parasitized by Cotesia glomerata, but the parasitism rate of Pieris brassicae larvae tends to be lower than that of Pieris rapae. To examine the process of parasitizing Pieris brassicae larvae, we observed how the parasitoid wasp responded to the host larvae on damaged leaves. Cotesia glomerata females tended to avoid Pieris brassicae larvae, and even when female wasps inserted their ovipositors into Pieris brassicae larvae, none laid eggs. The parasitoids obtained from Pieris rapae larvae failed to parasitize Pieris brassicae during the host-acceptance step.     

Comparative headspace analysis of cabbage plants damaged by two species ofPieris caterpillars: consequences for in-flight host location byCotesia parasitoids

Headspace composition, collected from intact cabbage plants and cabbage plants infested with eitherPieris brassicae L. orP. rapae L. (Lepidoptera: Pieridae) first instar larvae, was determined by GC-MS. Twenty-one volatiles were identified in the headspace of intact plants. Twenty-two volatiles were identified in the headspace of plants infested byP. brassicae larvae, 2 of which, Z-3-hexenyl butyrate and Z-3-hexenyl isovalerate, were not detected in the headspace of either intact orP. rapae damaged plants. In the headspace of the latter, 21 compounds were identified, all of which which were also produced by intact plants. No significant quantitative differences were found between headspace composition of the plants damaged by one or the other caterpillar species. Major differences between intact and caterpillar-damaged plants in contribution to the headspace profile were revealed for hexyl acetate, Z-3-hexenyl acetate, myrcene, sabinene and 1,8-cineole. The larval endoparasitoidCotesia glomerata L. was attracted by the volatiles emanating fromB. oleracea damaged byP. brassicae first instar larvae.C. rubecula L., a specialized larval endoparasitoids ofP. rapae, was attracted by the volatiles released from theB. oleracea-P. rapae plant-host complex. This shows that cabbage plants kept under the conditions of headspace collection produce attractive volatiles for both parasitoids.     

Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction

We tested whether a plant's life time seed production is increased by parasitization of herbivores in a tritrophic system, Arabidopsis thaliana (Brassicaceae) plants, Pieris rapae (Lepidoptera: Pieridae) caterpillars and the solitary endoparasitoid Cotesia rubecula (Hymenoptera: Braconidae). We established seed production for intact A. thaliana plants, plants that were mechanically damaged, plants fed upon by parasitized caterpillars and plants fed upon by unparasitized caterpillars. In the first experiment, with ecotype Landsberg (erecta mutant), herbivory by unparasitized P. rapae caterpillars resulted in a strongly reduced seed production compared to undamaged plants. In contrast, damage by P. rapae caterpillars that had been parasitized by C. rubecula did not result in a significant reduction in seed production. For the second experiment with the ecotype Columbia, the results were identical. Plants damaged by unparasitized caterpillars only produced seeds on regrown shoots. Seed production of plants that had been mechanically damaged was statistically similar to that of undamaged plants. Production of the first ripe siliques by plants fed upon by unparasitized caterpillars was delayed by 18–22 days for Landsberg and 9–10 days for Columbia. We conclude that parasitization of P. rapae by C. rubecula potentially confers a considerable fitness benefit for A. thaliana plants when compared to plants exposed to feeding damage by unparasitized P. rapae larvae. Plants that attract parasitoids and parasitoids that respond to herbivore-induced plant volatiles will both experience selective advantage, justifying the use of the term mutualism for this parasitoid-plant interaction. This type of mutualism is undoubtedly very common in nature.     

Host selection and larval interactions among three primary parasitoids ofPlathypena scabra (Lep.: noctuidae)

Three hymenopteran parasitoids that attackPlathypena scabra (F.) larvae often oviposit into consecutive instars of the host. We investigated host discrimination by adults and competitive interactions among larvae of these three parasitoid species. Avoidance of superparasitism byCotesia marginiventris (Cresson) andDiolcogaster facetosa Ashmead was tested. Females of each species were presented either withP. scabra parasitized by a different female of the same species 6 h earlier or unparasitizedP. scabra. Under these conditions,C. marginiventris attacked similar numbers of parasitized and unparasitized hosts.D. facetosa attacked 31% fewer parasitized than unparasitizedP. scabra. The avoidance of multiple parasitism byD. facetosa was studied in a similar bioassay. AlthoughD. facetosa females parasitized fewerP. scabra that had been attacked byC. marginiventris 6 h previously, the reduction in parasitism was only about 23%. In competition studies, immatureD. facetosa were better competitors than immatureC. marginiventris. Aleiodes (=Rogas) nolophanae (Ashmead) was an inferior competitor against bothC. marginiventris andD. facetosa when the duration between parasitism events was 1 h, but their competitive ability increased when they multiply parasitized hosts at least 32 h after the initial oviposition.     

Coexistence and niche segregation by field populations of the parasitoids Cotesia glomerata and C. rubecula in the Netherlands: predicting field performance from laboratory data

Field experiments with foraging parasitoids are essential to validate the conclusions from laboratory studies and to interpret differences in searching and host selection behaviour of parasitoid species. Furthermore, field experiments can indicate whether the parameters measured in the laboratory are relevant to elucidation of the ecological processes under study, such as adaptation or species interactions. In previous extensive laboratory studies we studied plant- and host-searching behaviour, host acceptance, host suitability; host plant preference, and learning of two congeneric parasitoids of Pieris caterpillars: the generalist Cotesia glomerata, which has been reported to attack several Pieridae species, and C. rubecula, a specialist of the small cabbage white Pieris rapae. In the present field study our aim was to verify the importance of these previous laboratory findings for explaining the performance of these two species in the field. We investigated experimentally whether parasitism on three Pieris species varied with parasitoid species and with food plant of the caterpillars. We exposed different types of host plants, infested with different Pieris species, to parasitism by natural populations of Cotesia species, by setting the experimental plants out in Brussels sprouts cabbage fields. Furthermore we made direct observations of parasitoid foraging in the field. In general, the field results confirmed our predictions on the range of host plant and host species used in the field. The two Cotesia species appear to coexist through niche segregation, since C. glomerata was mainly recovered from P. brassicae and C. rubecula from P. rapae. Although C. glomerata is a generalist at the species level, it can be a specialist at the population level under certain ecological circumstances. Our study shows the importance of variation in host plant attraction and host species acceptance in restricting host plant and host diet in the field. Furthermore the results suggest that, at least in the Netherlands, specialisation of C. glomerata on P. brassicae may occur as a result of C. rubecula outcompeting C. glomerata in P. rapae larvae. Received: 8 July 1999 / Accepted: 31 January 2000     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.     

Innate responses of the parasitoidsCotesia glomerata andC. rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes

To determine and compare innate preferences of the parasitoid speciesCotesia glomerata andC. rubecula for different plant-herbivore complexes, long-range (1-m) foraging behavior was studied in dual-choice experiments in a wind tunnel. In this study we tested the hypothesis that naive females of the specialistC. rubecula should show more pronounced preferences for different plant-herbivore complexes than females of the generalistC. glomerata. The herbivore species used were the pieridsPieris brassicae, P. rapae, P. Napi, andAporia crataegi and the nonhostsPlutella xylostella andMamestra brassicae. All herbivore species feed mainly on cabbage and wild crucifers, exceptAporia crataegi, which feeds on species of Rosaceae. Both parasitoid species preferred herbivore-damaged plants over nondamaged plants. NeitherC. rubecula norC. glomerata discriminated between plants infested by different caterpillar species, not even between plants infested by host-and nonhost species. Both parasitoid species showed preferences for certain cabbage cultivars and plant species. No differences were found in innate host-searching behavior betweenC. glomerata andC. rubecula. The tritrophic system cabbage-caterpillars-Cotesia sp. seems to lack specificity on the herbivore level, whereas on the plant level differences in attractiveness to parasitoids were found.     

Observations on the oviposition behaviour ofGoniozus sensorius [Hymenoptera: Bethylidae] a parasite ofDiaphania indica [Lepidoptera: Pyralidae]

Goniozus sensorius Gordh (Hymenoptera: Bethylidae) was recorded as a major parasite of the pumpkin caterpillar,Diaphania indica (Saunders) (Lepidoptera: Pyralidae). This paper provides detailed information on the oviposition behaviour ofG. sensorius. Prior to oviposition, the parasite temporarily paralyses the host larva. The paralysed condition lasts for about 2 h. The egg laying process on each larva requires 30 to 60 min. The maximum number of eggs are laid on the 6^th and 7^th segment, and none in the terminal segments. Generally, oviposition is restricted to 1 segment of the host larva and occasionally on 3 segments. The maximum number of eggs are laid on the 2^nd and 3^rd day after emergence and the mean number of eggs laid on each host larva was 7.1.     

Host suitability of the New World stalkborer Diatraea considerata for three Old World Cotesia parasitoids

Biological control ofstalkboring Lepidoptera often has beensuccessful when the braconid parasitoids in thegenera Cotesia and Apanteles werethe natural enemies of choice. Constraints inusing these gregarious, koinobiont,endoparasitoids have included host suitability,especially as influenced by the host's immuneresponse. The suitability of a novel host, theNew World stalkborer Diatraeaconsiderata (Lepidoptera:Pyralidae), for parasitization by three OldWorld braconids, Cotesia chilonis, C. flavipes and C. sesamiae (Hymenoptera: Braconidae), wascompared to the suitability of another NewWorld novel host, Diatraea saccharalis. D. considerata was less suitable for allthree parasitoids than was D.saccharalis. The frequent occurrence ofparasitized D. considerata larvae thatdid not yield parasitoids, or pupate within anappropriate time interval, suggestedencapsulation of the parasitoid progeny, whichwas visible through the host cuticle. Giventhe suitability results, these threeparasitoids would not be appropriate candidatesfor use against D. considerata. Theresults also have important implications forthe narrow host range expressed by theseparasitoids.