Life history traits and foraging behaviour of Cotesia nonagriae (Olliff) (Hymenoptera: Braconidae), a newly recognised member of the Cotesia flavipes complex of stemborer parasitoids

Cotesia nonagriae (Olliff) from Australia, a parasitoid of the incidental native pest of sugarcane, Bathytricha truncata (Walker) (Lepidoptera: Noctuidae), was previously thought to be a synonym of Cotesia flavipes Cameron. However, recent studies using DNA sequences, morphology and preliminary biological information show that this parasitoid is clearly a different species than C. flavipes and other members of the species complex. Here we further examine differences in the biology of these species by undertaking a detailed study of the life history traits of C. nonagriae , including adult longevity and the potential and realised fecundity of females. In addition, the influence of learning on microhabitat location and foraging behaviour were investigated. Duration of the larval stages and adult longevity of C. nonagriae were longer than previously recorded for other members of the species complex. The potential fecundity of females was similar to C. flavipes (∼200 eggs); however, C. nonagriae oviposited a average of over 100 eggs into each host, almost three times more than for other species in the C. flavipes complex (30–40). The propensity of C. nonagriae to allocate a large number of eggs to each host may be an evolutionary strategy due to the high mortality rate (50–57%) of ovipositing adult wasps. During microhabitat location, both naïve and experienced females demonstrated a strong response towards the plant host complex, with experienced wasps benefiting by having a more rapid response time to host-induced volatiles and cues.     

Influence of plant structural complexity on the foraging success of Trichogramma minutum: a comparison of search on artificial and foliage models

The influence of structural complexity on the foraging success for host eggs (Ephestia kuehniella Zeller) by Trichogramma minutum Riley was investigated in the laboratory. Naive females were released into arenas with structurally different paper models or foliage (simple: trembling aspen Populus tremuloides Michx., complex: balsam fir Abies balsamea L.). Observations of individual females were made every 15 min and searching success was measured by the number of host egg clusters found and the amount of time taken to find them, within a period of 196 min. Females found significantly more egg clusters and were quicker at finding them on the sample paper and foliage surfaces than on the most complex paper or foliage surfaces. Older females (2–3 days) were more successful and searched quicker than younger (<24 h) females on all paper surfaces. The timed observations suggested that wasps which spent more time walking had a significantly decreased probability of finding an egg mass and were significantly slower at finding them. Females that spent more time on paper surfaces had an increased probability of finding an egg mass. The significance of searching differences is discussed in relation to the potential effects of plant surfaces on Trichogramma movements and to the physiological readiness of the wasp.     

Fitness of two sibling species of Asobara (Braconidae:Alysiinae), larval parasitoids of Drosophilidae in different microhabitats

Abstract. 1. Two sibling species of larval endoparasitoids of Drosophilidae: Asobara tabida (Nees) and A.rufescens (Foerster) occur in the same macrohabitat, but inhabit different microhabitats. Each species is most attracted by odours of its own microhabitat.
2. In order to assess the adaptive value of the microhabitat preference we studied the survival of both parasitoids in the major host species that occur in these microhabitats.
3. Survival in the major host in the preferred microhabitat was shown to be 40% higher for A.tabida and 30% higher for A.rufescens when compared to survival in the major host in the non-preferred microhabitat.
4. Measurements of developmental rates, specific mortalities and dry weights of the parasitoids suggest that the differential survival is due to differences in synchronization with the hosts.
5. The possible evolutionary consequences of some biological characteristics in Asobara are discussed. Microhabitat selection, differential survival, development and mating behaviour are attributes likely to have played a role in the reduction of gene flow between populations of the ancestral species, either in primary or in secondary sympatry.     

Comparison of learning in related generalist and specialist eucoilid parasitoids

Effects of learning in two microhabitat specialists, Leptopilina boulardia Barbotin et al. and L. fimbriata Kieffer were compared to previous and new results of learning in the microhabitat generalist L. heterotoma Thomson. Females were given one or more oviposition experiences on hosts in different types of substrate. In all species oviposition experience affected the choice for a substrate, although this effect of learning was considerably less in L. fimbriata compared to the other two species. Patch times, known to be highly determined by experience in the generalist L. heterotoma, were much less flexible in the specialists. L. boulardi and L. fimbriata have fixed patch times on their natural substrate and have variable patch times on other substrates only. In all three species one oviposition affected the choice for a substrate. Additional ovipositions showed no different effect. An accumulative effect of the number of ovipositions on patch times was found in L. heterotoma only. Retention of the learning effect was only studied in L. boulardi, and was shown to be similar to that reported for L. heterotoma, i.e. two to three days. Although learning was found in both the generalist and the specialist species studied, it seems to affect their foraging behaviour differently.     

Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth

Mating has profound effects on animal physiology and behaviour, not only in females but also in males, which we show here for olfactory responses. In cotton leafworm moths, Spodoptera littoralis, odour-mediated attraction to sex pheromone and plant volatiles are modulated after mating, producing a behavioural response that matches the physiological condition of the male insect. Unmated males are attracted by upwind flight to sex pheromone released by calling females, as well as to volatiles of lilac flowers and green leaves of the host plant cotton, signalling adult food and mating sites, respectively. Mating temporarily abolishes male attraction to females and host plant odour, but does not diminish attraction to flowers. This behavioural modulation is correlated with a response modulation in the olfactory system, as shown by electro-physiological recordings from antennae and by functional imaging of the antennal lobe, using natural odours and synthetic compounds. An effect of mating on the olfactory responses to pheromone and cotton plant volatiles but not to lilac flowers indicates the presence of functionally independent neural circuits within the olfactory system. Our results indicate that these circuits interconnect and weigh perception of social and habitat odour signals to generate appropriate behavioural responses according to mating state.     

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

Host locating behaviour of Leschenaultia exul and Patelloa pachypyga: two tachinid parasitoids of the forest tent caterpillar, Malacosoma disstria

Leschenaultia exul (Townsend) and Patelloa pachypyga (Aldrich & Webber) (Diptera: Tachinidae) are the principal larval parasitoids of the forest tent caterpillar (FTC) Malacosoma disstria (Hübner) (Lepidoptera: Lasiocampidae) in Canada. The response of these two fly species to M. disstria differs depending on the tree species on which the host feeds. In wind tunnel experiments, L. exul spent more time on the side of the tunnel containing volatiles from FTC frass and was attracted to the FTC-aspen poplar (Populus tremuloides Michx.) complex preferentially to the FTC-balsam poplar (Populus balsamifera L.) complex. Field bioassays confirmed that this fly species was preferentially attracted to the herbivore-aspen poplar complex as compared to the herbivore-balsam poplar complex. In field bioassays, P. pachypyga was also attracted preferentially to aspen poplar trees containing FTC larvae, compared to balsam poplar trees with host larvae.     

Orientation responses of the grasshopper, Melanoplus sanguinipes, to visual, olfactory and wind stimuli and their combinations

Prereproductive adults of the grasshopper, Melanoplus sanguinipes (F.) (Orthoptera, Acrididae), demonstrated orientation and movement towards both visual and olfactory stimulus sources in a still-air chamber. Visual stimuli (wheat and lima bean foliage, vertical black or yellow-green stripes, and a yellow-green broad leaf pattern) were approached more frequently than the control white background surface. Olfactory stimuli (chopped wheat foliage and a four-component, synthetic, grass odor blend of volatiles) elicited an even greater positive response than the visual stimuli. Changing the proportions of the four volatiles in the blend significantly reduced positive orientation responses to the stimulus source. Visual cues of wheat foliage and olfactory cues of either chopped wheat odor or the grass odor blend gave greater responses when combined than when presented separately.In flowing air or wind, nearly all insects demonstrated a rapid positive response to odors of chopped wheat and the grass odor blend, significantly greater than the response to the same stimuli in still air. However, positive responses to visual cues were not significantly greater in wind than in still air. When combined with the olfactory stimuli in flowing air, visual cues did not increase the incidence of response. Grasshoppers responding to grass odors in wind moved more rapidly and directly toward the source, and stopped less often and for shorter durations than insects responding to odor in still air or to visual cues.We conclude from these studies that M. sanguinipes adults show orientation behavior to both visual and olfactory stimuli from food plant sources, although leaf odors elicit a stronger positive response particularly when carried by wind.     

Visual and olfactory responses of haematophagous Diptera to host stimuli

Key biotic and environmental constraints on the host-orientated behaviour of haematophagous Diptera are summarized. For each major group of biting Diptera, responses to host stimuli are reviewed, including activation and ranging behaviour, long-range and short-range olfactory responses and visual responses. Limitations to the comparison of results between groups of species, and the practical problems of experimental method and equipment are discussed.     

The influence of light and moisture gradients on the attack rate of parasitoids foraging for hosts in a laboratory arena (Hymenoptera: Pteromalidae)

Microhabitat preferences of four parasitoids (Hymenoptera: Pteromalidae) of house fly pupae were measured in a two-dimensional arena containing perpendicular light and moisture gradients. Parasitism by Muscidifurax raptorand Nasonia vitripenniswas greatest in dry substrates, with the latter preferring bright illumination and the former tending to prefer dark. Urolepis rufipesselected bright illumination and moist substrates, attacking the most hosts at bright-moist and dim-moist microhabitats. Spalangia cameroniexhibited no main-effect preference for light intensity or moisture, although parasitism was highest at dim-moist, dark-wet, and dark-moist microhabitats. These results demonstrate that simple abiotic attributes, such as light intensity and substrate moisture concentration, are important in defining some dimensions of the niches of these parasitoids.     

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.     

Monoclonal antibodies specific for Laelius pedatus (bethylidae) and Bracon hebetor (braconidae), two hymenopterous parasitoids of stored-product pests

Before parasitoids and predators are fully endorsed as biological control agents in storage facilities, a reliable technique must be developed to determine how much they contribute to the overall insect contamination of stored commodities. Because determining the origin of insect fragments by visual examination is difficult, labor-intensive, and requires special skills, we propose using immunological techniques to differentiate among insect species biochemically. In the example presented here, we generated monoclonal antibodies (MAbs) against the parasitic wasps Laelius pedatus (Say) and Bracon hebetor Say. The MAbs reacted with all life stages and both sexes of the parasitoids. In Western blots of acrylamide and agarose gels, the MAbs recognized high molecular weight proteins (>500 kDa) composed of multiple subunits, with mildly acidic to neutral isoelectric focusing points. The MAbs did not cross-react with the additional 22 insect species we tested in an indirect enzyme-linked immunosorbent assay. These data suggest that MAb-based immunoassays could be used to differentiate among beneficial and destructive insects found in stored products.     

Host preferences of two encyrtid parasitoids for the Columbian Phenacoccus spp. of cassava mealybugs

In a choice test among six life stages of Phenacoccus herreni Cox & Williams, Epidinocarsis diversicornis (Howard) used its antennae to examine adult and 3rd stadium females more than other stages and preferentially attempted to oviposit in these plus 2nd stadium females. Success of ovipositor insertion was unaffected by host stage. The outcome of these behaviors was preferential oviposition by E. diversicornis in the large female host stages. Acerophagus coccois Smith also preferentially examined larger female mealybugs (second and third stadium nymphs and adults) more than other stages and successfully inserted its ovipositor in these stages more often than in second stadium male nymphs and male cocoons, resulting in a similar preference in this species for larger female host stages. When given a choice between adult female hosts of two species, P. herreni and Phenacoccus gossypii Townsend & Cockerell, E. diversicornis exhibited a clear preference for P. herreni; whereas A. coccois preferred P. gossypii.

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Résumé Epidinocarsis diversicornis (Howard), ayant la possibilité de choisir entre six stades différents de Phenacoccus herreni Cox & Williams, examine avec ses antennes plus particulièrement les adultes et les larves femelles du 3ème stade, et essaie de pondre de préférence dans ces stades et les larves femelles de second stade. L'insertion de la tarière s'effectue aussi bien quel que soit le stade de l'hôte. Il résulte de ces différents aspects du comportement que E. diversicornis pond de préférence dans les femelles des stades les plus avancés. Acerophagus coccois Smith préfère aussi examiner les cochenilles femelles les plus grosses (second et 3ème stade larvaires et adulte), et introduit sa tarière avec succès dans ces stades plus souvent que dans les larves mâles de second stade ou les cocons mâles; il en résulte aussi pour cette espèce une préférence pour les femelles des stades les plus gros.Quand on leur a donné le choix entre des femelles des deux espèces de cochenilles (P. herreni et Phenacoccus gossypii Towsend & Cockerell), E. diversicornis manifestait une nette préférence pour P. herreni, tandis que A. coccois préférait P. gossypii.

     

Temperature-dependent growth rates for the cassava mealybug, Phenacoccus herreni, and two of its encyrtid parasitoids, Epidinocarsis diversicornis and Acerophagus coccois in Colombia

Developmental rates for Phenacoccus herreni Cox & Williams were determined at 18°, 20°, 22°, 25°, 30° and 35°C for the egg, all juvenile male and all juvenile female stadia. Longevity was determined for adult females and adult males. Developmental rates for the P. herreni parasitoid Epidinocarsis diversicornis (Howard) were determined at 18°, 20°, 25° and 30°C for the oviposition-to-mummy-formation period and the mummy-formation-to-adult-eclosion period. Developmental rates were determined for the P. herreni parasitoid Acerophagus coccois Smith for the same two life stages at 20°, 25° and 30°C. Least-squares-derived polynomial equations or logistic equations were fitted to each data set (except for A. coccois) so that rates could be interpolated for temperatures between observed points for use in an analysis of the impact of these parasitoids on population dynamics of P. herreni. Results of this analysis are presented separately.

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Résumé Les vitesses de développement des oeufs et de tous les stades larvaires mâles et femelles de P. herreni Cox & Williams ont été déterminées à 18°, 20°, 22°, 25°, 30° et 35°C. La longévité des adultes mâles et femelles a été déterminée. Les vitesses de développement de la ponte à la formation du cocon et de celleci à l'émergence de E. diversicornis Howard, encyrtide parasite de P. herreni ont été déterminées à 18°, 20°, 25° et 30°C. Il en a été de même pour un second encyrtide parasite A. coccois Smith à 20°, 25° et 30°C. Les équations polynomiales des derniers carrés dérivés et les équations logistiques ont été ajustées pour chaque lot de données (à l'exception de A. coccois) de façon à ce qu'elles aient pu être interpolées pour analyser l'impact de ces parasites sur la dynamique de population de P. herreni. Les résultats de cette analyse sont présentés à part.

     

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.     

Post-release survey to assess impact and potential host range expansion by Amitus hesperidum and Encarsia perplexa, two parasitoids introduced for the biological control of the citrus blackfly, Aleurocanthus woglumi in Dominica

Four years after the release of two exotic parasitoids, Amitus hesperidum Silvestri (Hymenoptera: Platygasteridae) and Encarsia perplexa Huang and Polaszek (Hymenoptera: Aphelinidae) for the classical biological control of the citrus blackfly (CBF), Aleurocanthus woglumi Ashby (Hemiptera: Aleyrodidae) in Dominica, a survey was conducted to assess establishment as well as potential nontarget effects especially on Aleyrodidae and other related taxa. CBF populations were low to non-existent in 50 of 51 field sites examined. At the site where CBF was encountered, both E. perplexa and A. hesperidum were present and CBF populations were declining. The two parasitoids were not among the several species collected on nontarget Aleryodidae and Hemiptera. It is concluded that E. perplexa and A. hesperidum have kept CBF populations under effective biological control in Dominica and there is no evidence of any nontarget effects on other Aleyrodidae or their natural enemies. Handling Editor: Dirk Babendreier.