Parasitoid Load Research Articles

Multi-Species Host Use by the Parasitoid Fly Ormia lineifrons.

Antagonistic species relationships such as parasitoid/host interactions lead to evolutionary arms races between species. Many parasitoids use more than one host species, requiring the parasitoid to adapt to multiple hosts, sometimes being the leader or the follower in the evolutionary back-and-forth between species. Thus, multi-species interactions are dynamic and show temporary evolutionary outcomes at a given point in time. We investigated the interactions of the multivoltine parasitoid fly Ormia lineifrons that uses different katydid hosts for each of its fly generations sequentially over time. We hypothesized that this fly is adapted to utilizing all hosts equally well for the population to persist. We quantified and compared the fly's development in each of the four Neoconocephalus hosts. Cumulative parasitism rates ranged between ~14% and 73%, but parasitoid load and development time did not differ across host species. Yet, pupal size was lowest for flies using N. velox as a host compared to N. triops and other host species. Successful development from pupa to adult fly differed across host species, with flies emerging from N. triops displaying a significantly lower development success rate than those emerging from N. velox and the other two hosts. Interestingly, N. triops and N. velox did not differ in size and were smaller than N. robustus and N. nebrascensis hosts. Thus, O. lineifrons utilized all hosts but displayed especially low ability to develop in N. triops, potentially due to differences in the nutritional status of the host. In the multi-species interactions between the fly and its hosts, the poor use of N. triops may currently affect the fly's evolution the most. Similarities and differences across host utilization and their evolutionary background are discussed.

Rearing temperature and parasitoid load determine host and parasitoid performance in Manduca sexta and Cotesia congregata

1. Temperature strongly influences the rates of physiological processes in insects, including the herbivore Manduca sexta and its larval endoparasitoid Cotesia congregata. Parasitisation by C. congregata decreases the growth and consumption of food by larval M. sexta. However, the effects of temperature on parasitised caterpillars and the developing wasp larvae are largely unknown.2. In this study, parasitised and unparasitised caterpillars were reared at three constant temperatures (20, 25 and 30 °C) throughout larval development. Caterpillar mass gain and consumption were monitored daily until wandering (unparasitised control group) or wasp emergence (parasitised group) was observed. Development time and survival to emergence were measured as metrics of parasitoid performance.3. Parasitised M. sexta developed more slowly than unparasitised controls, but had similar cumulative consumption until the terminal instar. Parasitised caterpillars with relatively large parasitoid loads had higher rates of consumption and growth than those with smaller loads. Both temperature and parasitoid load strongly affected wasp success. Mean development time to wasp emergence increased with low temperatures and with large loads. The combination of warm temperature and large parasitoid loads greatly reduced wasp survival.4. These results demonstrate the interactive effects of rearing temperature and parasitisation on host consumption and growth rates throughout larval development. In addition, wasp performance was affected by the interaction of temperature and parasitoid load size. High temperatures alter the dynamics of the interaction between the parasitoid and its caterpillar host, which could have far‐reaching impacts as the global temperatures continue to rise.

Immunity of leaf-cutting ants and its role in host-parasitoid relationships

Parasites are an important selection pressure for all organisms, and host immune responses are key in shaping host-parasite interactions. Host species with strong immune defences may be expected to experience lower parasitism; on the other hand, investment in immune function is costly, so hosts that have evolved to invest more in immune defence may be expected to have been under greater selection pressure from parasites. Disentangling the coevolutionary dynamics requires comparative studies that quantify the immune responses of potential hosts of parasites in a community, but such studies are rare. Here, we studied the immune defences of six leaf-cutting ant species in a community for which their relationships with phorid fly parasitoid species are known. We tested whether the strength of the baseline immune defences of the different ant species correlated positively or negatively with parasitoid load (number and abundance of parasitoid species exploiting the ant species), and host specialization of parasitoid species (the proportion of specialist parasitoids using each host). We measured four immune variables: i) the encapsulation response to a standard challenge, levels of ii) phenoloxidase (PO) and iii) prophenoloxidae (PPO) immune enzymes, and iv) the number of haemocytes. We found that ant species differed in their encapsulation response, PO levels and number of haemocytes, and that there was a positive, not negative, correlation across ant species between the strength of several of the immune variables and parasitoid load, but not for host specialization. This is in keeping with the hypothesis that higher parasitoid load selects for greater investment in immune defences. Our results suggest that immunity may be an important factor accounting for the dynamics of host-parasitoid interactions in this community. Similar community-level studies may be insightful, both for understanding host-parasite community ecology and for applications such as biocontrol.

Differential Nest Parasitism in Three Sympatric Social Wasps (Hymenoptera: Vespidae: Polistes spp.) in the West Indies

Jamaica's three species of social wasps were found nesting together in a suburban area. Their nests gave evidence of markedly different parasitoid loads in the sequence Polistes crinitus > P. dorsalis > P. major . Based on larval and pupal silk remains, the moth Chalcoela pegasalis appears to be the main nest parasitoid at this locality. Despite widely different parasitoid loads, the estimated per-nest production of adults was similar among the three species. This suggests a trade-off between investment in anti-parasitoid tactics and in other brood-care activities.

Infection behavior, life history, and host parasitism rates of Emblemasoma erro (Diptera: Sarcophagidae), an acoustically hunting parasitoid of the cicada Tibicen dorsatus (Hemiptera: Cicadidae).

'Eavesdropping' parasitoids find their hosts by homing in on the communication signals of other insects. These parasitoids often exploit chemical communication, but at least some species of the sarcophagid genusEmblemasomaeavesdropon the acoustic communications of cicadas. Despite considerable scientific interest in acoustic parasitoids, we know remarkably little about most species of Emblemasoma. To better understand the ecology and behavioral diversity of these flies, I used a combination of field and laboratory techniques to elucidate theinfection behavior and life history of E.erro,which uses the cicada Tibicen dorsatusasa host, and I also investigated parasitoid loads and parasitism rates of T.dorsatus inmultiple host populations in the central United States. Female E. erro used the acoustic signals of male T. dorsatus as the primary means of locating hosts, but they also required physical movement by the host, usually either walking or flight, to provide visual cues for the final larviposition attack. Larvae were deposited directly on the host's integument and burrowed through intersegmental membrane to enter the host's body. On average, E. erro larvae spent 88.0 h residing inside their host before leaving to pupariate, but residence time was strongly dependent on both ambient temperature and effective clutch size. Adult flies eclosed about 18 days after pupariation. Across all study sites, the mean parasitoid load of infected male T. dorsatus was 4.97 larvae/host, and the overall parasitism rate was 26.3%. Parasitism rates and parasitoid loads varied considerably amonghost population samples, and high parasitism rates were usually associated with high parasitoid loads. Previously, detailed information about the infection behavior, life history, and host parasitism rates of sarcophagid acoustic parasitoids was only available for one species, E. auditrix. This study reveals that the infection behavior of E. erro is quite different from that of E. auditrix and, more broadly, unlike that known for any other species of acoustic parasitoid. The life histories of these two Emblemasoma are also divergent. These differences suggest that sarcophagid acoustic parasitoids are more behaviorally and ecologically diverse than previously recognized and in need of further study.

Parasitoid load affects plant fitness in a tritrophic system

AbstractPlants attacked by herbivorous insects emit volatile compounds that attract predators or parasitoids of the herbivores. Plant fitness increases when these herbivorous insects are parasitized by solitary parasitoids, but whether gregarious koinobiont parasitoids also confer a benefit to plant fitness has been disputed. We investigated the relationship between parasitoid load of the gregarious Cotesia glomerata (L.) (Hymenoptera: Braconidae), food consumption by larvae of their host Pieris brassicae L. (Lepidoptera: Pieridae), and seed production in a host plant, Brassica nigra L. (Brassicaceae), in a greenhouse experiment. Plants damaged by caterpillars containing single parasitoid broods produced a similar amount of seeds as undamaged control plants and produced significantly more seeds than plants with unparasitized caterpillars feeding on them. Increasing the parasitoid load to levels likely resulting from superparasitization, feeding by parasitized caterpillars was significantly negatively correlated with plant seed production. Higher parasitoid brood sizes were negatively correlated with pupal weight of Cotesia glomerata, revealing scramble competition leading to a fitness trade‐off for the parasitoid. Our results suggest that in this tritrophic system plant fitness is higher when the gregarious parasitoid deposits a single brood into its herbivorous host. A prediction following from these results is that plants benefit from recruiting parasitoids when superparasitization is prevented. This is supported by our previous results on down‐regulation of synomone production when Brassica oleracea was fed on by parasitized caterpillars of P. brassicae. We conclude that variable parasitoid loads in gregarious koinobiont parasitoids largely explain existing controversies about the putative benefit of recruiting these parasitoids for plant reproduction.

PARASITES AND SEXUAL REPRODUCTION IN PSYCHID MOTHS

Persistence of sexual reproduction among coexisting asexual competitors has been a major paradox in evolutionary biology. The number of empirical studies is still very limited, as few systems with coexisting sexual and strictly asexual lineages have been found. We studied the ecological mechanisms behind the simultaneous coexistence of a sexually and an asexually reproducing closely related species of psychid moth in Central Finland between 1999 and 2001. The two species compete for the same resources and are often infected by the same hymenopteran parasitoids. They are extremely morphologically and behaviorally similar and can be separated only by their reproductive strategy (sexual vs. asexual) or by genetic markers. We compared the life-history traits of these species in two locations where they coexist to test predictions of the cost-of-sex hypothesis. We did not find any difference in female size, number of larvae, or offspring survival between the sexuals and asexuals, indicating that sexuals are subject to cost of sex. We also used genetic markers to check and exclude the possibility of Wolbachia bacteria infection inducing parthenogenesis. None of the samples was infected by Wolbachia and, thus, it is unlikely that these bacteria could affect our results. We sampled 38 locations to study the prevalence of parasitoids and the moths' reproductive strategy. We found a strong positive correlation between prevalence of sexual reproduction and prevalence of parasitoids. In locations where parasitoids are rare asexuals exist in high densities, whereas in locations with a high parasitoid load the sexual species was dominant. Spatial distribution alone does not explain the results. We suggest that the parasite hypothesis for sex may offer an explanation for the persistence of sexual moths in this system.

The effects of host weight at parasitism on fitness correlates of the gregarious koinobiont parasitoid Microplitis tristis and consequences for food consumption by its host, Hadena bicruris

AbstractGregarious koinobiont parasitoids attacking a range of host sizes have evolved several mechanisms to adapt to variable host resources, including the regulation of host growth, flexibility in larval development rate, and adjustment of clutch size. We investigated whether the first two mechanisms are involved in responses of the specialist gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) to differences in the larval weight and parasitoid load of its host Hadena bicruris Hufn. (Lepidoptera: Noctuidae). In addition, we examined the effects of parasitism on food consumption by the host. Parasitoids were offered caterpillars of different weight from all five instars, and parasitoid fitness correlates, including survival, development time, and cocoon weight, were recorded. Furthermore, several host growth parameters and food consumption of parasitized and unparasitized hosts were measured. Our results show that M. tristis responds to different host weights by regulating host growth and by adjusting larval development rate. In hosts with small weights, development time was increased, but the increase was insufficient to prevent a reduction in cocoon weight, and as a result parasitoids experienced a lower chance of successful eclosion. Cocoon weight was negatively affected by parasitoid load, even though host growth was positively affected by parasitoid load, especially in hosts with small weights. Later instars were more optimal for growth and development of M. tristis than early instars, which might reflect an adaptation to the life‐history of the host, whose early instars are usually concealed and inaccessible for parasitism on its food plant, Silene latifolia Krause (Caryophyllaceae). Parasitism by M. tristis greatly reduced total host food consumption for all instar stages. Whether plants can benefit directly from the attraction of gregarious koinobiont parasitoids of their herbivores is a subject of current debate. Our results indicate that, in this system, the attraction of a gregarious koinobiont parasitoid can directly benefit the plant by reducing the number of seeds destroyed by the herbivore.

Nontarget Effect of Entomophagous Biocontrol: Shared Parasitism Between Native Lepidopteran Parasitoids and the Biocontrol AgentTrigonospila brevifacies(Diptera: Tachinidae) in Forest Habitats

The parasitoid guild attacking preimaginal Tortricidae on shrubs and small trees in broadleaf/podocarp forests was studied at six sites in the central North Island. Connectance and quantitative webs were used to interpret the complexities of host parasitoid interactions at a community level and identify competition between native parasitoids and the introduced species Trigonospila brevifacies (Hardy). Trigonospila brevifacies is numerically dominant in the tortricid parasitoid guild. Its host range overlaps with 12 native and one introduced parasitoid species, and it parasitizes more species of Tortricidae than other parasitoids at the North Island forest sites surveyed. Quantification of the parasitoid load on native Lepidoptera indicated that T. brevifacies parasitism comprised between 15.6 and 79.5% of the parasitoid load per species. Only the introduced Australian canefruit pest Eutorna phaulocosma Meyrick (Lepidoptera: Oecophoridae) received a higher proportion of parasitism from T. brevifacies than any of the native Lepidoptera. The number of parasitoid species attacking each preimaginal host stage (except for pupae) of native Lepidoptera was relatively constant. The only pupal parasitoid recorded was the introduced ichneumonid Xanthopimpla rhopaloceros Krieger (Hymenoptera: Ichneumonidae). All native parasitoid species were less abundant than T. brevifacies.

Teratocytes of microplitis rufiventris in superparasitized host larvae

The effects of superparasitism on the size and number of teratocytes (giant cells released by the serosa of braconid eggs after hatching) found in the host Spodoptera littoralis at the completion of development of the solitary endoparasitoid Microplitis rufiventris were assessed. Although the number of teratocytes increased, on average, with parasitoid load (1, 2 or 3 parasitoid eggs), this increase was lower than predicted, based on the number of parasitoids (i.e., is not proportional to parasitoid load). Similarly, the size of the teratocytes decreased as a function of parasitoid load. The total volume of the teratocytes (mm3) is reduced by 39.1 and 66.4% in hosts parasitized twice and three times, respectively. It is concluded that, in superparasitized hosts, some form of competition likely takes place among the teratocytes, or between these cells and the first‐hatched larva, possibly through the action of a chemical (released by the latter) that inhibits the growth of teratocytes from supernumerary parasitoids. In singly parasitized hosts 73.2, 17.8 and 9.0% of total teratocytes were found in hosts abdomen, head capsule and thoracic regions, respectively. In superparasitized hosts, the cells tended also to collect in the posterior region of the host but with fewer number of cells in the head capsule. It seems that the teratocytes possibly act as a biological regulating factor to adjust host's endocrine system for successful development of the parasitoid.

Nutritional ecology of the interaction between larvae of the gregarious ectoparasitoid, Muscidifurax raptorellus (Hymenoptera: Pteromalidae), and their pupal host, Musca domestica (Diptera: Muscidae)

In this study we examined the relationship between clutch size and parasitoid development of Muscidifurax raptorellus (Hymenoptera: Pteromalidae), a gregarious idiobiont attacking pupae of the housefly, Musca domestica (Diptera: Muscidae). Host quality was controlled in the experiments by presenting female parasitoids with hosts of similar size and age. This is the first study to monitor the development of a gregarious idiobiont parasitoid throughout the course of parasitism. Most female wasps laid clutches of one to four eggs per host, although some hosts contained eight or more parasitoid larvae. In both sexes, parasitoids completed development more rapidly, but emerging adult wasp size decreased as parasitoid load increased. Furthermore, the size variability of eclosing parasitoid siblings of the same sex increased with clutch size. Irrespective of clutch size, parasitoids began feeding and growing rapidly soon after eclosion from the egg and this continued until pupation. However, parasitoids in hosts containing five or more parasitoid larvae pupated one day earlier than hosts containing one to four larvae. The results are discussed in relation to adaptive patterns of host utilization by gregarious idiobiont and koinobiont parasitoids.

Inhibition of testicular growth and development in Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata

Tobacco hornworm larvae parasitized by the gregarious larval endoparasitoid Cotesia congregata exhibited an inhibition in testicular growth and development, the extent of which was determined by the age and developmental stage of the host at the time of parasitization. The degree of parasitic castration, as assessed by measurements of testicular volume, was correlated with the stadium in which parasitization occurred. A mathematical formula requiring the measurement of testicular length, width and depth was used to calculate testicular volume. The use of the depth parameter revealed a negative correlation between host weight and testicular volume in parasitized larvae. Testicular volumes of fifth instar hosts, which had been parasitized in the first stadium, were significantly smaller than those originally parasitized as fourth or fifth instar larvae and were not correlated with parasitoid load. Effects of natural parasitism were not duplicated by injections of C. congregata polydnavirus and venom, topical treatment with the juvenile hormone analog methoprene, or starvation of nonparasitized larvae. Larvae receiving virus plus venom or methoprene grew larger due to delayed wandering and had larger testes than controls. Deleterious effects on host testes may be due to the effects of nutrient competition between the developing parasitoid progeny and the gonads, combined with the juvenilizing effects believed to be caused by the polydnavirus.

Colony size and parasitoid load in two species of colonial Metepeira spiders from Mexico (Araneae: Araneidae).

While a number of advantages may result from group living, it may also lead to increased levels of attack by parasites because groups may be easier to find. This leads to the prediction that levels of parasitism should increase with colony size. We test this prediction by comparing colony size and parasitoid load for two species of colonial orb-weaving spiders from Mexico, Metepeira (undesc. sp., tentatively named atascadero) and Metepeira incrassata, which exhibit contrasting levels of social organization and utilize different habitats. For M. atascadero, which occurs solitarily or in small groups in desert/mesquite grassland habitat, rates of egg-sac parasitism fluctuate widely from year to year, and are closely tied to spider egg output. There is no relationship between colony size and rate of parasitism. For colonial M. incrassata, which occur in tropical rain forest/agricultural habitat, rates of parasitism are relatively constant from year to year. However, there is a positive relationship between colony size and rate of parasitism in this species. These differences are discussed with regard to the stability of the two habitats, prey availability, and the foraging behavior of the respective parasitoids.

Seed predation in the legume Crotalaria : II. Correlates of interplant variability in predation intensity.

Correlates of individual plant escape from seed predation were investigated for an East African population of the shrub Crotalaria pallida (Papilionaceae) in which seed mortality due to chewing insects is high and varies among neighboring individuals. Several plant properties expected to influence phytophagous insect host choice or fitness were measured simultaneously and their contribution to variance in predation examined with multiple regression analysis. Microhabitat, seed pyrrolizidine alkaloid concentration, and parasitoid load on the seed predators are the best predictors of predation intensity; plant size, distance from conspecifics, and infructescence characteristics do not appear to affect predation probabilities. However, predictions of the direction of microhabitat effects were only partially successful, and contrary to expectation, plants with higher seed alkaloid levels experienced greater seed predation; several hypotheses are advanced to account for these results. Higher parasitoid loads are associated with lower predation intensity, probably due in part to interference between lepidopteran larvae and the less voracious hymenopteran seed predators or their parasitoids.