Postemergence learning in the insect parasitoid,Cotesia congregata (Say) (Hymenoptera: Braconidae)

Exposing newly emerged females of Cotesia congregata(Say) to wild cherry, an inherently unattractive plant, and their host larvae at 0–4 h after adult emergence induced a positive searching response to wild cherry and an inhibited response to cabbage, an attractive plant. Inherent responses were not affected when females were exposed to their hosts at 0–12 h and to cherry at 8–12 h after emergence. The induced response to cherry was constant until its disappearance at 6–7 days;inhibition of the response to cabbage was released at 4–5 days after emergence. Postemergence exposure to cherry and parasitoid cocoons induced similar but weaker searching responses. Induced searching responses exhibit features of associative learning and receptor modification. In addition to its presumed role in foraging, postemergence experience with plants may encourage assortative mating of C. congregatawithin suitable host habitats and, thus, facilitate local adaptations to specific plants.     

Effects of postemergence experience on searching and landing responses of the insect parasitoid,Cotesia congregata (Say) (Hymenoptera: Braconidae), to plants

Postemergence experience with one of six plant species, in the presence of the host larva, modified the searching response of reproductively mature females of Cotesia congregata(Say) to these plants in at least one of three ways: (1) an increased response to the plant experienced at emergence, (2) an increased response to other plants, or (3) an inhibited response to other plants. Landing and searching responses were differentially affected by postemergence experience. For example, postemergence experience with tobacco (a common plant) in the presence of the host larva induced a landing preference for this plant over parsley (a novel plant) but did not affect searching responses to either plant, whereas experience with parsley and the host larva induced an increased searching response to parsley but a landing preference for tobacco. Differential effects of postemergence experience may reflect the type of stimuli involved in searching or landing and may have adaptive significance.     

Effects of the polydnavirus of Cotesia congregata on the immune system and development of non-habitual hosts of the parasitoid

Polydnaviruses (PDV) are obligate mutualistic symbionts found in association with some groups of parasitic Hymenoptera. In these groups, they suppress the immune response of the parasitoid’s host and are required for successful parasitoid reproduction. Several PDV effects have been described in different experimental systems, but no clear picture of PDV mode of immunosuppression has emerged. No study to date has directly tested if PDV modes of action are evolutionarily conserved or divergent among parasitoid taxa within the Ichneumonoidea. We hypothesize the divergence in PDV mode of immunosuppression can be detected by identifying points of divergence in the immune response of different host species to PDV from one parasitoid species. This study tests the effects of purified PDV from Cotesia congregata on the immune response of three larval lepidopteran species that naturally are hosts of parasitoid species that differ in taxonomic relatedness to C. congregata. Here we demonstrate that despite associations with distantly related parasitoids (Ichneumonidae and Braconidae), Manduca sexta and Heliothis virescens showed similar patterns of increased glucose dehydrogenase (GLD) activity, suppressed cellular encapsulation in vitro, and increased time to pupation. In contrast, Lymantria dispar showed no response to C. congregata PDV across any of the parameters measured, even though it has an evolutionary association with several parasitoids closely related to C. congregata and within the Microgastrinae. The PDV immunosuppression in H. virescens and M. sexta does not correlate with host molecular phylogeny either. The suborganismal effects shown in M. sexta and H. virescens translated into significantly reduced pupation success in M. sexta only. Results demonstrate that while some PDV modes of immunosuppression in hosts may be divergent, others may be conserved across broad host groups.     

When good bugs go bad: intraguild predation by Jalysus wickhami on the parasitoid, Cotesia congregata

We report a case of direct intraguild predation involving an insect predator and parasitoid in an agricultural system. The spined stilt bug, Jalysus wickhami Van Duzee, feeds on eggs of the tobacco hornworm, Manduca sexta L., and also on prepupal and pupal stages of the gregarious hornworm parasitoid, Cotesia congregata (Say). In two separate trials, mean mortality of attached parasitoids was significantly lower (66%, 73%) than that of their detached siblings (97%, 96%) after a 3 day exposure to stilt bugs, demonstrating that attachment to the host offered some protection against predation. In no-choice experiments, prepupal parasitoids suffered greater mortality (0 day-old=61%, 1 day-old=65%) than pupal parasitoids (2 day-old=50%, 3 day-old=14%). When offered in combination with 0 or 2 day-old hornworm eggs, respective mortality of 0, 1, 2 and 3-day-old pupal parasitoids showed a similar pattern (67%, 63%, 33% and 23%). In another experiment, mortality of 0-day-old pupal parasitoids (64%) was greater than that of 3 day-old pupal parasitoids (38%). Mortality of pupal parasitoids was not affected by the availability of hornworm eggs, a highly acceptable food. Younger pupal parasitoids (=prepupae) probably suffered greater mortality because they were more easily fed on by stily bugs than older (pupated) ones. Because C. congregata overwinters in the prepupal stage, it may be particularly vulnerable to attack late in the season when stilt bug populations are large and hornworm eggs are relatively uncommon.     

Characterization of microsatellite loci in the parasitoid,Cotesia congregata (Say) (Hymenoptera Braconidae)

Nine microsatellite loci were developed and assayed for polymorphism in four groups of the insect parasitoid, Cotesia congregata (Say) (Hymenoptera). One locus was monomorphic and eight were polymorphic in C. congregata. Allelic distributions differed significantly between groups of C. congregata collected from solanaceous and catalpa host food plants (P = 0). Loci were tested for cross‐reactivity to six congeners: C. acuminata (Reinhard), C. bignellii (Marshall), C. cynthiae (Nixon), C. euphydryidis (Musebeck), C. koebelei (Riley) and C. melitaearum (Wilkinson). In the congeners, eight loci were polymorphic, four of which yielded allele sizes that differed substantially from sizes of amplification products observed for C. congregata.     

Influence of dietary nicotine and colony source ofManduca sexta [Lepidoptera: Sphingidae] on its suitability as a host ofCotesia congregata [Hymenoptera: Braconidae]

Larval tobacco hornworms,Manduca sexta (L.), of 2 different colonies were exposed to parasitism by the gregarious endoparasitoid,Cotesia congregata (Say). A comparison was made of parasitoid larval, pre-pupal, and pupal mortality, female and male dry weight and larval development time. In general, “Maryland” hornworms were more suitable hosts than “North Carolina” hornworms. Although the presence of dietary nicotine increased parasitoid mortality in individuals reared from hornworms of both colonies, the effect was more severe among individuals parasitizing the North Carolina hornworms. Scientific contribution No. 8125, article No. A-5066 of the Maryland Agricultural Experiment Station, Department of Entomology.     

Parasitism of an insect Manduca sexta L. alters feeding behaviour and nutrient utilization to influence developmental success of a parasitoid

The effects of macronutrient balance on nutrient intake and utilization were examined in Manduca sexta larvae parasitized by Cotesia congregata. Insects fed an artificial diet having constant total macronutrient, but with varied ratios of protein and carbohydrate, with altered diet consumption in response to excesses and deficiencies of the individual macronutrients. Bivariate plots of protein and carbohydrate consumption for non-parasitized larvae demonstrated a curvilinear relationship between points of nutrient intake for the various diets, and the larvae grew best on carbohydrate-biased diets. The relationship was linear for parasitized larvae with the growth uniform across diets. On protein-biased diets, the larvae regulated the nitrogen content, containing similar amounts of nitrogen regardless of consumption. Efficiency of nitrogen conversion in non-parasitized larvae was greatest on carbohydrate-biased diets, while nitrogen conversion by parasitized larvae was greatest with intermediate nutrient ratios. Accounting for carbohydrate consumption, the lipid content decreased as dietary carbohydrate increased, but parasitized larvae contained significantly less lipid. The total biomass of parasites developing in individual host larvae was positively correlated with host protein consumption, but the individual parasites were similar in size. Parasitism influences host nutrient consumption in a manner that achieves uniform host growth under diverse nutritional regimes, thereby constraining blood nutrient concentrations within limits suitable for parasite growth and development.     

Feeding behaviour and nutrient selection in an insect <Emphasis Type="Italic">Manduca sexta</Emphasis> L. and alterations induced by parasitism

Manduca sexta L. larvae exhibit broad food acceptance with regard to nutrient content during the first 3 days of the last stadium. Larvae fed diets with a constant combined level of casein and sucrose, but variable ratios, display a linear relationship between protein and carbohydrate intake. Larvae grow best on a diet with equal nutrients, but will consume an excess of one nutrient in order to obtain an adequate amount of the other, as nutrient ratio shifts. Parasitized larvae feed similarly, but the nutrient ratio does not affect growth. Unparasitized larvae regulate intake of protein and carbohydrate when offered choices of protein-biased and carbohydrate-biased diets having combined nutrient levels of 120 g/l, but with variable ratios. Larvae normally consume equal amounts of nutrients, regardless of ratio, and grow similarly. As combined nutrient level is reduced in one diet, larvae abandon regulation and feed randomly. Parasitized larvae offered choice diets with 120 g/l combined nutrients do not regulate nutrient intake. Consumption of nutrients varies widely, but growth is unaffected. Larvae offered choices of diets having equal amounts of casein and sucrose but variable fat (corn oil), fail to regulate fat intake, although both unparasitized and parasitized larvae prefer a diet containing higher fat.     

Dispersal of the exotic parasitoid Cotesia flavipes in a new ecosystem

A study on the dispersal of the exotic larval endoparasitoid, Cotesia flavipes Cameron (Hymenoptera: Braconidae), was conducted in a maize field in the northern Kilifi District in the coastal area of Kenya. Because C. flavipes did not previously occur in the release area, it was possible to use a unique indirect method to estimate dispersal by examining the distribution of parasitised hosts. Parasitoids released in the centre of the field moved as far as 64 meters during their life span, and dispersal was dependent on wind direction. The level of parasitism was influenced by the location of hosts in plants. The majority of parasitised stemborers (88.4%) were found inside the plant (stems and tassel stems), where 74.3% of the suitable hosts were found, which indicates that female parasitoids were not searching randomly for hosts. Aggregation of parasitoids in response to plants with different host densities was not detected. Implications of the release of C. flavipes on stemborers population in the agroecosystem of East Africa are discussed.     

Behavioral manipulation of host caterpillars by the primary parasitoid wasp Cotesia glomerata (L.) to construct defensive webs against hyperparasitism

Many parasitoids control the behavior of their hosts to achieve more preferable conditions. Decreasing predation pressure is a main aim of host manipulation. Some parasitoids control host behavior to escape from their enemies, whereas others manipulate hosts into constructing defensive structures as barriers against hyperparasitism. Larvae of the parasitoid wasp Cotesia glomerata form cocoon clusters after egression from the parasitized host caterpillar of the butterfly Pieris brassicae. After the egression of parasitoids, the perforated host caterpillar lives for a short period and constructs a silk web that covers the cocoon cluster. We examined whether these silk webs protect C. glomerata cocoons against the hyperparasitoid wasp Trichomalopsis apanteroctena. In cocoon clusters that were not covered by silk webs (bare clusters), only cocoons hidden beneath others avoided hyperparasitism. In covered cocoon clusters, both cocoons hidden beneath others and those with a space between them and the silk web avoided hyperparasitism, whereas cocoons that contacted the silk webs were parasitized. The frequency of cocoons that were hidden beneath others increased with the increasing number of cocoons in a cluster, but the defensive effect of cluster size was thought to be lower than that of silk webs. However, the rate of hyperparasitism did not differ between covered and bare clusters when we allowed the hyperparasitoids to attack the cocoon clusters in an experimental arena. This result was thought to have been caused by low oviposition frequency by these hyperparasitoids. As a result, silk webs did not guard the cocoons from hyperparasitoids in our experiments, but would protect cocoons under high hyperparasitism pressure by forming a space through which the ovipositors could not reach the cocoons.     

Manipulation of fifth-instar host (Manduca sexta) ecdysteroid levels by the parasitoid wasp Cotesia congregata

Although 5th (last) instar parasitized Manduca sexta larvae undergo developmental arrest and do not wander, they exhibit a small hemolymph ecdysteroid peak (300-400pg/&mgr;l) which begins one day prior to the parasitoid's molt to the 3rd (last) instar and concomitant emergence from the host. Ecdysteroids present in this peak were 20-hydroxyecdysone, 20,26-dihydroxyecdysone and one or more very polar ecdysteroids, as well as small amounts of 26-hydroxyecdysone and ecdysone. In parasitized day-1 and -2 5th instars ligated just behind the 1st abdominal proleg, hemolymph ecdysteroid levels increased in both anterior and posterior portions (100-500pg/&mgr;l), while in unparasitized larvae, hormone levels only increased in the anterior portion (100-350pg/&mgr;l). Thus, the ecdysteroid peak observed in host 5th instars was probably produced, at least in part, by the parasitoids. It may serve to promote Cotesia congregata's molt from the second to the third instar and/or to facilitate parasitoid emergence from the host. In parasitized day-1 and -2 5th instars ligated between the last thoracic and 1st abdominal segments, hemolymph ecdysteroid titers reached much higher levels (500-3500pg/&mgr;l) in the anterior portion (no parasitoids present) than in the posterior portion (150-450pg/&mgr;l). Therefore, it appears that the parasitoid's regulation of hemolymph ecdysteroid titers occurs at two levels. First, parasitization neutralizes the host's ability to maintain its normal hemolymph ecdysteroid levels. Second, in a separate action, the parasitoid manipulates the ecdysteroid-producing machinery so that hemolymph levels are maintained at the 200-400pg/&mgr;l characteristic of day 3-4 hosts. This is the first report of a parasitoid's ability to interfere with the normal inhibitory mechanisms which prevent prothoracic gland production of ecdysteroid at inappropriate periods of insect growth and development.     

Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata

The relative suitability of four host plants was determined both for unparasitized Pieris brassicae L. caterpillars and for Cotesia glomerata (L.) developing in P. brassicae. For unparasitized P. brassicae, growth rate and pupal weight were highest on Brussels sprouts and Swedish turnip, intermediate on rape, and lowest on nasturtium. In contrast, C. glomerata larval developmental rate and adult longevity were greatest for wasps from P. brassicae reared on nasturtium.On all four plants, the host-parasitoid complex attained a lower final weight than unparasitized P. brassicae, and it is argued that this difference is due primarily to reduced consumption by parasitized P. brassicae. Among parasitized caterpillars, however, complex weight was positively correlated with clutch size, suggesting that C. glomerata larvae are able to partially counteract the effect of parasitization per se on host consumption.The host plants of P. brassicae appear to face an evolutionary dilemma: in order to increase the total mass of parasitoids produced, they must suffer greater loss of foliage. This trade-off, if common in nature, may represent a formidable constraint on coevolution between host plants and parasitoids.     

Effects of potassium levels over the range occurring in host plants on the growth of an insect herbivore (Manduca sexta)

Third instar tobacco hornworms (Manduca sexta L.: Sphingidae) on low dietary potassium had a lower relative growth rate than individuals on diets with potassium concentrations reflecting those in host-plants, due to decreased consumption rate, lower efficiencies of conversion of ingested and digested food (ECI and ECD), and a prolonged growth/feeding phase. Furthermore, these larvae, when placed on a diet with a moderate potassium concentration through the fourth stadium, ended up being smaller due to lower ECI and less biomass gained, and had a prolonged growth phase, which suggest an irreversible cost of the previous low potassium diet. Third instar hornworms on high potassium diets had lower ECI and ECD, and they had a prolonged growth phase. These individuals, when placed on a moderate potassium diet in the fourth stadium, gained less biomass, than those previously offered hostplant-like-potassium diets. Body potassium concentrations (% dw) at the end of the third stadium were similar among treatment groups. With increasing potassium concentrations in the diet, utilization efficiencies of potassium decreased and potassium concentrations in the frass increased. Correspondingly, water content (% fw) of the newly-molted fourth instar larvae declined with increasing potassium, indicating a passive loss of water during potassium excretion. Low and high dietary potassium reduced survivorship of third instar larvae; fourth instar caterpillars previously fed the low potassium diet also had poor survivorship. We conclude that, within the normal range of potassium concentrations in the hostplants, caterpillar performance is largely unaffected by potassium concentration, but that potassium-poor and potassium-rich diets, such as those hornworms may sometimes experience, can reduce growth and survivorship.     

Genetic Variation in Behavioral Response to Herbivore-Infested Plants in the Parasitic Wasp, Cotesia glomerata (L.) (Hymenoptera: Braconidae)

Female Cotesia glomerata (L.) relies on stimuli from herbivore-infested plants to select suitable hosts, but behavioral response to such stimuli is highly variable among individuals. This study investigates a genetic component of phenotypic variability in both short-range host-search and long-range host-location behaviors in the tritrophic system consisting of cabbage plants (Brassica oleracea L.), cabbage butterfly (Pieris brassicae L.) and the parasitoid, by comparing full-sib families established from a laboratory population and isofemale strains from a field population. Short-range host-search behaviors were examined within a Petri-dish test arena, and long-range host-location behaviors assessed in a wind tunnel. Significant differences among full-sib families were shown in the duration of walking on a plant-herbivore complex (i.e., a leaf section with two host caterpillars, their silk and feces) and searching off the complex, and the total time elapsed for wasps to locate a host larva after release into the test arena. Flight responses to and landing choices between the intact and the herbivore-infested plants were also significantly different among these families. Effects of families on both short-range host-search and long-range host-location behaviors were consistent, without significant influences of host larvae from which wasps emerged. The analysis of isofemale strains reveals that strains account for significant variation in the oriented flight response to herbivore-infested plants, and the isofemale heritability for this behavioral character is estimated as 0.447. The results suggest that genetic variation exists at different behavioral levels of the host-selection process in this parasitoid.     

Activity-dependent induction of facilitation,depression, and post-tetanic potentiation at an insect central synapse

Summary In Manduca sexta larvae, sensory neurons innervating planta hairs on the tips of the prolegs make monosynaptic excitatory connections with motoneurons innervating proleg retractor muscles. Tactile stimulation of the hairs evokes reflex retraction of the proleg. In this study we examined activity-dependent changes in the amplitude of the excitatory postsynaptic potentials (EPSPs) evoked in a proleg motoneuron by stimulation of individual planta hair sensory neurons. Deflection of a planta hair caused a phasic-tonic response in the sensory neuron, with a mean peak instantaneous firing frequency of >300 Hz, and a tonic firing rate of 10–20 Hz. Direct electrical stimulation was used to activate individual sensory neurons to fire at a range of frequencies including those observed during natural stimulation of the hair. At relatively low firing rates (e.g., 1 Hz), EPSP amplitude was stable indefinitely. At higher instantaneous firing frequencies (>10 Hz), EPSPs were initially facilitated, but continuous stimulation led rapidly to synaptic depression. High-frequency activation of a sensory neuron could also produce post-tetanic potentiation, in which EPSP amplitude remained elevated for several min following a stimulus train. Facilitation, depression, and post-tetanic potentiation all appeared to be presynaptic phenomena. These activity-dependent changes in sensory transmission may contribute to the behavioral plasticity of the proleg withdrawal reflex observed in intact insects.Abbreviations ACh acetylcholine - AChE acetylcholine esterase - CNS central nervous system - EPSP excitatory postsynaptic potential - I _h injected hyperpolarizing current - LTP long-term potentiation - PPR principal planta retractor motoneuron - PTP post-tetanic potentiation - R _in input resistance - V _h hyperpolarized potential - V _m membrane potential - VN ventral nerve - VNA anterior branch of the ventral nerve - V _r resting potential.     

Intrinsic competition between the gregarious parasite,Cotesia glomeratus and the solitary parasite.Cotesia rubecula [Hymenoptera: Braconidae] for their host.Artogeia rapae [Lepidoptera: Pieridae]

The solitary endoparasite,Cotesia rubecula, was superior to the gregarious endoparasite,Cotesia glomeratus, in tests of intrinsic competition for their hostArtogeia rapae. When an egg ofC. rubecula was oviposited in the host prior to those ofC. glomeratus, C. rubecula always won the ensuing competition. When an egg ofC. rubecula was laid in the same host within 48 h after oviposition byC. glomeratus, C. rubecula was successful in more than 90% of the interactions. Even when the egg ofC. rubecula was oviposited in the same host 72 to 96 h after oviposition byC. glomeratus, C. rubecula won the competition approximately 33% of the time. The implications of intrinsic competition are discussed in relation to the establishment ofC. rubecula in an ecosystem containingA. rapae andC. glomeratus.      

Inhibition of Telenomus sphingis an egg parasitoid of Manduca spp. by trichome/2-tridecanone-based host plant resistance in tomato

The resistance of accession PI 134417 of the wild tomato Lycopersicon hirsutum f. glabratum C. H. Mull to Manduca sexta (L.) (Lepidoptera: Spingidae) and Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) is conditioned by the high densities of 2-tridecanone-containing, glandular trichomes associated with the foliage. In laboratory experiments, rates of parasitism of M. sexta eggs by Telenomus sphingis (Ashmead) (Hymenoptera: Scelionidae) were lower among eggs on PI 134417 foliage than among eggs on foliage of the cultivated tomato L. esculentum Mill. (cv. Better Boy). The latter is characterized by a significantly lower density of type VI glandular trichomes than PI 134417 and an absence of 2-tridecanone. Parasitism by T. sphingis was also reduced among eggs on foliage of the F₁ hybrid between PI 134417 and L. esculentum. The hybrid foliage lacks 2-tridecanone but has a density of type VI glandular trichomes that is intermediate between those of PI 134417 and L. esculentum, indicating that elevated densities of type VI glandular trichomes adversely affect T. sphingis. This conclusion was further substantiated by the finding that there were no differences among plant lines in the levels of parasitism of M. sexta eggs when the eggs were on foliage that had been divested of glandular trichomes.In bioassays in which T. sphingis adults or immatures in host eggs were exposed to filter paper treated with 2-tridecanone at rates comparable to those associated with PI 134417 foliage, 2-tridecanone was acutely toxic and caused high levels of mortality. In addition, at high concentrations, 2-tridecanone vapors were repellent to T. sphingis adults. However, when exposed to PI 134417 foliage, few T. sphingis adults were killed.Parasitism of M. sexta eggs was unaffected when the eggs were deposited by moths reared as fifth instar larvae on diet containing 2-tridecanone and/or 2-undecanone at levels comparable to those associated with PI 134417 foliage.