Ecology Of Parasitoids Research Articles

Tapping for love: courtship, mating, and behavioral asymmetry in two aphid parasitoids, Aphidius ervi and Aphidius matricariae (Hymenoptera: Braconidae: Aphidiinae).

Understanding the biology and ecology of parasitoids can have direct implications for their evaluation as biological control agents, as well as for the development and implementation of mass-rearing techniques. Nonetheless, our current knowledge of the possible influence of lateralized displays (i.e., the asymmetric expression of cognitive functions) on their reproductive behavior is scarce. Herein, we characterized the behavioral elements involved in courtship, and quantified the durations of 2 important aphid parasitoids, Aphidius ervi Haliday and Aphidius matricariae Haliday (Hymenoptera: Braconidae: Aphidiinae). We quantified the main indicators of copulation and examined the occurrence of lateralized traits at population level. Results indicated that A. matricariae exhibited longer durations of wing fanning, antennal tapping, pre-copula and copula phases compared to A. ervi. Postcopulatory behavior was observed only in A. matricariae. Unlike other parasitoid species, the duration of wing fanning, chasing, and antennal tapping did not affect the success of the mating of male A. ervi and A. matricariae. Both species exhibited a right-biased female kicking behavior at the population level during the pre-copula. Our study provides insights into the fundamental biology of aphidiine parasitoids and reports the presence of population-level lateralized mating displays, which can serve as useful benchmarks to evaluate the quality of mass-rearing systems.

Nest visitors of Vespula wasps and their potential use for biological control in an invaded range

The common and the German wasp, Vespula vulgaris and V. germanica, have proved to be prolific invasive species capable of degrading local ecosystems and costing invaded countries millions of dollars annually. Despite clear incentive, control strategies are yet to have any significant deleterious impact on invasive populations. Several species of arthropods are known to inhabit Vespula nests and feed upon developing larvae as either parasitoids or predators. Recent control strategies propose the use of such parasitoids as agents of biocontrol against invasive wasps (Volucella inanis in particular). Despite a general understanding of parasitoid ecology, some aspects such as prevalence, distribution, and behaviour remain limited. Here, we surveyed natural enemy prevalence in wasp nests over the period of three years and we tested larvae prey preference of two Volucella species, V. inanis and V. zonaria towards Vespula wasps. We find V. inanis to be the most prevalent of four prominent candidates for Vespid biocontrol—V. inanis, V. zonaria, Sphecophaga vesparum, and Metoecus paradoxus. Using two-choice assays, we find larvae of V. inanis to have slight yet significant prey preference for V. vulgaris larvae over V. germanica larvae, whilst V. zonaria display no preference. Furthermore, V. inanis were not averse to still predating upon V. germanica, doing so in 41% of trials. Prior exposure has no effect on the prey-preference. Our work provides experimental evidence that V. inanis is a promising candidate for biocontrol of invasive Vespula wasps, as the larvae predate on both target species of Vespula and display no exclusive preference among them.

Parasitoid ecology along geographic gradients: lessons for climate change studies.

One method to study the impact of climate change on host-parasitoid relationships is to compare populations along geographical gradients in latitude, altitude, or longitude. Indeed, temperatures, which vary along geographic gradients, directly shape the life traits of parasitoids and indirectly shift their populations through trophic interactions with hosts and plants. We explored the pros and cons of using these comparisons along gradients. We highlighted that the longitudinal gradients, although understudied, are well correlated to winter warming and summer heat waves and we draw attention to the impact of the increase in extreme events, which will probably be the determining parameters of the effect of climate change on host-parasitoid relationships.

Competitive interactions in insect parasitoids: effects of microbial symbionts across tritrophic levels.

Competition for hosts is a common ecological interaction in insect parasitoids. In the recent years, it has become increasingly evident that microorganisms can act as 'hidden players' in parasitoid ecology. In this review, we propose that parasitoid competition should take into consideration the microbial influence. In particular, we take a tritrophic perspective and discuss how parasitoid competition can be modulated by microorganisms associated with the parasitoids, their herbivore hosts, or the plants attacked by the herbivores. Although research is still in its infancy, recent studies have shown that microbial symbionts can modulate the contest outcome. The emerging pattern is that microorganisms not only affect the competitive traits of parasitoids but also the fighting arena (i.e. the herbivore host and its food plant), in which competition takes place. We have also identified important gaps in the literature that should be addressed in future studies to advance our understanding about parasitoid competition.

The Biology and Ecology of Parasitoid Wasps of Predatory Arthropods.

Parasitoid wasps are important components of insect food chains and have played a central role in biological control programs for over a century. Although the vast majority of parasitoids exploit insect herbivores as hosts, others parasitize predatory insects and arthropods, such as ladybird beetles, hoverflies, lacewings, ground beetles, and spiders, or are hyperparasitoids. Much of the research on the biology and ecology of parasitoids of predators has focused on ladybird beetles, whose parasitoids may interfere with the control of insect pests like aphids by reducing ladybird abundance. Alternatively, parasitoids of the invasive ladybird Harmonia axyridis may reduce its harmful impact on native ladybird populations. Different life stages of predatory insects and spiders are susceptible to parasitism to different degrees. Many parasitoids of predators exhibit intricate physiological interrelationships with their hosts, adaptively manipulating host behavior, biology, and ecology in ways that increase parasitoid survival and fitness.

Resting ecology of parasitoids in the field: safe in a bed and breakfast?

The selection of a safe place to rest at night may be an essential survival strategy for diurnal animals. Despite the importance of parasitoid wasps as consumers in terrestrial ecosystems, their selection of sites to rest and their mortality during the night have not been measured, to the best of our knowledge, reflective of a general lack of understanding of resting behaviours of insects in the field. Here, we used parasitoid wasps of the genus Aphytis (Hymenoptera: Aphelinidae), the highly successful biological control agents of the California red scale, Aonidiella aurantii (Hemiptera: Diaspididae), to study the resting ecology of parasitoids in the field over space and time, considering both external and internal correlates of parasitoid resting behaviour. At night, Aphytis wasps tended to rest on citrus tree leaves, which have a lower host density, but also fewer predators and a greater density of food sources for adult wasps, compared to fruit and branches. On this plant substrate, most of the population avoided predators and survived the night. Aphytis wasps selected leaves on which to rest at night in a nonrandom fashion. They tended to aggregate on leaves with high densities of hosts and food sources (honeydew) and with low densities of potential predators. During the day, wasps with lower egg loads tended to remain on leaves, likely resting and maturing eggs. Overall, our results demonstrate, for the first time, that parasitoids select certain sites at which to rest safely at night. These findings also suggest that the availability of safe resting places could be a valuable resource for beneficial insects in agroecosystems, especially those that have life spans extending over multiple days. • Diurnal insects search for places to rest safely at night. • We studied the resting ecology of Aphytis parasitoids in the field. • At night, they aggregated on leaves with high densities of hosts and food sources. • Parasitoids avoided resting on leaves with potential predators. • More than 90% of the parasitoids avoided predator attacks and survived the night.

Extrinsic Inter- and Intraspecific Competition in Parasitoid Wasps

The diverse ecology of parasitoids is shaped by extrinsic competition, i.e., exploitative or interference competition among adult females and males for hosts and mates. Adult females use an array of morphological, chemical, and behavioral mechanisms to engage in competition that may be either intra- or interspecific. Weaker competitors are often excluded or, if they persist, use alternate host habitats, host developmental stages, or host species. Competition among adult males for mates is almost exclusively intraspecific and involves visual displays, chemical signals, and even physical combat. Extrinsic competition influences community structure through its role in competitive displacement and apparent competition. Finally, anthropogenic changes such as habitat loss and fragmentation, invasive species, pollutants, and climate change result in phenological mismatches and range expansions within host-parasitoid communities with consequent changes to the strength of competitive interactions. Such changes have important ramifications not only for the success of managed agroecosystems, but also for natural ecosystem functioning.

Modeling Climatic Influences on Three Parasitoids of Low-Density Spruce Budworm Populations. Part 1: Tranosema rostrale (Hymenoptera: Ichneumonidae)

Despite their importance as mortality factors of many insects, the detailed biology and ecology of parasitoids often remain unknown. To gain insights into the spatiotemporal biology of insect parasitoids in interaction with their hosts, modeling of temperature-dependent development, reproduction, and survival is a powerful tool. In this first article of a series of three, we modeled the biology of Tranosema rostrale at the seasonal level with a three-species individual-based model that took into account the temperature-dependent performance of the parasitoid and two of its hosts. The predicted activity of the first adult parasitoid generation closely matched the seasonal pattern of attack on the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). The model predicted 1–4 full generations of T. rostrale per year in eastern North America. The generations were generally well synchronized with the occurrence of larvae of a probable alternate host, the obliquebanded leafroller Choristoneura rosaceana (Lepidoptera: Tortricidae), which could be used as an overwintering host. Spatial differences in predicted performance were caused by complex interactions of life-history traits and synchrony with the overwintering host, which led to a better overall performance in environments at higher elevations or along the coasts. Under a climate warming scenario, regions of higher T. rostrale performance were predicted to generally move northward, making especially lower elevations in the southern range less suitable.

How climate change affects the seasonal ecology of insect parasitoids

1. In the context of global change, modifications in winter conditions may disrupt the seasonal phenology patterns of organisms, modify the synchrony of closely interacting species and lead to unpredictable outcomes at different ecological scales.2. Parasites are present in almost every food web and their interactions with hosts greatly contribute to ecosystem functioning. Among upper trophic levels of terrestrial ecosystems, insect parasitoids are key components in terms of functioning and species richness. Parasitoids respond to climate change in similar ways to other insects, but their close relationship with their hosts and their particular life cycle – alternating between parasitic and free‐living forms – make them special cases.3. This article reviews of the mechanisms likely to undergo plastic or evolutionary adjustments when exposed to climate change that could modify insect seasonal strategies. Different scenarios are then proposed for the evolution of parasitoid insect seasonal ecology by exploring three anticipated outcomes of climate change: (i) decreased severity of winter cold; (ii) decreased winter duration; and (iii) increased extreme seasonal climatic events and environmental stochasticity.4. The capacities of insects to adapt to new environmental conditions, either through plasticity or genetic evolution, are highlighted. They may reduce diapause expression, adapt to changing cues to initiate or terminate diapause, increase voltinism, or develop overwintering bet‐hedging strategies, but parasitoids' responses will be highly constrained by those of their hosts.5. Changes in the seasonal ecology of parasitoids may have consequences on host–parasitoid synchrony and population cycles, food‐web functioning, and ecosystem services such as biological pest control.

Metabolomics of aging assessed in individual parasitoid wasps.

Metabolomics studies of low-biomass organisms, such as small insects, have previously relied on the pooling of biological samples to overcome detection limits, particularly using NMR. We show that the differentiation of metabolite profiles of individual 1 mg parasitoid wasps of different ages is possible when using a modified sample preparation and a combination of untargeted NMR and LC-MS based metabolomics. Changes were observed between newly emerged and older wasps in glycerolipids, amino acids and circulatory sugars. This advance in chemical profiling has important implications for the study of the behaviour and ecology of parasitoids and many other species of small organisms because predictions and observations are typically made at the level of the individual. Thus, the metabolomic state of low-biomass individuals can now be related to their behaviour and ecological performance. We discuss specifically the utility of age-related metabolomic profiling but our new approach can be applied to a wide range of biological research.

Antennal gustatory perception and behavioural responses in Trissolcus brochymenae females

Trissolcus brochymenae (Hymenoptera: Platygastridae) is an egg parasitoid that could be used to control stink bugs like Murgantia histrionica (Heteroptera: Pentatomidae), a pest of brassicaceous crops. Before laying their eggs, parasitoid females spend considerable time examining the substrate with their antennae, which are also used during feeding and mating behaviours. This suggests that contact chemoreception plays a prominent role in many aspects of parasitoid ecology. Therefore, we examined the sensitivity of antennal taste sensilla chaetica to several classical tastants including those that are appetitive or aversive. In addition we studied the taste preferences of wasps when presented with these chemicals alone or mixed. The sensilla chaetica of T. brochymenae responded to serial concentrations of sucrose, salts, and quinine, but no concentration-dependent effect was observed when testing sinigrin, a secondary metabolite found in many brassicaceae. However, both sinigrin and quinine inhibited responses to 0.1M sucrose when mixed with this sugar. Behavioural taste preference assays confirmed that wasps showed a dose dependent preference for sucrose over agarose. In addition, a behavioural avoidance of sucrose solutions containing quinine was observed. This effect was not observed when sinigrin was used as a feeding deterrent. In the two-choice tests the wasp did not discriminate between sucrose solutions mixed with salts and sucrose alone. Further no preference for salts or sinigrin compared to agarose alone was observed. This work represents the first step towards the identification of gustatory receptor neurons implicated in the detection of different types of chemical cues in egg parasitoids.

Sources of variation in larval parasitism of two sympatrically outbreaking birch forest defoliators

1. Studies of insect communities rarely support the parasitoid–host regulation hypothesis. Spatio-temporal variation in parasitoid prevalence due to complex food web interactions or abiotic factors may prevent parasitoids from regulating hosts. 2. We examined the relative contribution of spatial (altitude) and temporal (years) sources to total variation in parasitoid prevalence rates in outbreaks of Epirrita autumnata Borkhausen and Operophtera brumata Linnaeus populations. We tested whether prevalence rates of generalist parasitoids were correlated between sympatric host populations and to what extent any of the parasitoids were host density dependent. 3. Four larval parasitoids (two specialists and two generalists) exhibited significantly structured spatio-temporal dynamics over years and altitudes. The prevalence rates of one of the generalists were spatio-temporally correlated between the two host species, while for the other they were not. 4. Three parasitoids showed tendencies for direct or delayed positive density dependence as expected from numerical and functional responses to their hosts. However, the effects were weak and minute compared to the variation attributed to year and altitude. 5. We conclude that unknown aspects of the larval parasitoid ecology that co-vary with altitude and year in the study system dominate their prevalence dynamics and thus act to hinder density-dependent responses that could potentially regulate host populations.

The role of host plant species in the phenotypic differentiation of sympatric populations of Aleiodes nolophanae and Cotesia marginiventris

AbstractThe ecology of parasitoids is strongly influenced by their host plant species. Parasitoid fitness can be affected by a variety of plant traits that could promote phenotypic differentiation among populations of parasitoids. Generalist parasitoids are expected to be more affected by plant traits (e.g., plant defensive traits) than specialist parasitoids. Data are presented on phenotypic differences of two braconid parasitoid wasps ovipositing on the same insect host species on two different host plant species. Adult mass, adult longevity, and percent parasitism are compared for the generalist parasitoid Cotesia marginiventris Cresson and the specialist parasitoid Aleiodes nolophanae Ashmead (both Hymenoptera: Braconidae) emerging from green cloverworms, Hypena scabra Fabricius (Lepidoptera: Noctuidae), feeding on two host plant species, alfalfa (Medicago sativa L.) and soybean (Glycine max L. Merr.) (both Fabaceae), at three locations. Specialist wasps that parasitized the green cloverworm on alfalfa had a significantly larger mass than the ones that parasitized the green cloverworm on soybean at the three study sites. Generalist wasps that parasitized green cloverworms on alfalfa had a larger mass than wasps parasitizing green cloverworms on soybean only at one of the study sites (i.e., Prince George's County, MD, USA). Similarly, both specialist and generalist wasps lived longer when parasitizing green cloverworms on alfalfa than when parasitizing them on soybean at only one of the study sites (i.e., Prince George's County). In Prince George's County, percent parasitism on alfalfa by the specialist parasitoid was higher than on soybean for three consecutive years and percent parasitism by the generalist parasitoid was the same on alfalfa and soybean every year. Thus, phenotypic differences among populations associated with different host plant species vary geographically (i.e., parasitoid phenotype associated with different host plant species differ at some sites while it is the same at other sites). The implications of geographic variation for biological control are discussed.

Aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their associations related to biological control in Brazil

This study evaluated the parasitoid-aphid-plant associations in Brazil with the objective of developing a useful research database for further studies of aphid parasitoid ecology and aphid management. The original material was obtained from collections made in Paraná, Rio Grande do Sul, Minas Gerais, and São Paulo states. The published information on the Aphidiinae in Brazil is revised. The general features of the target parasitoid fauna of Central and South America is summarized and promising biological control programs of some aphid species in Brazil is discussed.

Effects of Millet, Wheat, Rice, and Sorghum Diets on Development of <I>Corcyra cephalonica</I> (Stainton) (Lepidoptera: Galleriidae) and Its Suitability as a Host for <I>Trichogramma chilonis</I> Ishii (Hymenoptera: Trichogrammatidae)

Emergence and survival of adults for 24 h was compared for Trichogramma chilonis Ishii reared on eggs of Corcyra cephalonica (Stainton) adults whose larval growth and development had been monitored on broken grains of four different cereals: finger millet (Eleusine coracana L. Gaertn), soft white wheat (Triticum aestivum L), short-grained white rice (Oryza sativa L.), and durra sorghum (Sorghum bicolor L. Moench). For C. cephalonica, the percentage adult emergence and several fifth-instar food use indices (consumption index, relative growth rate, and efficiencies of conversion of ingested and digested food) were significantly higher for millet-reared than for sorghum-reared larvae. The nutritional indices for wheat- and rice-reared C. cephalonica larvae were intermediate between the indices for larvae reared on millet and sorghum. The percentage adult emergence and percentage 24-h survival of T. chilonis were significantly higher on eggs of C. cephalonica hosts reared on millet than on eggs of those reared on sorghum. These results suggest that the rearing of C. cephalonica larvae on a high-quality nutritional source resulted in high-quality eggs, which ultimately resulted in high-quality T. chilonis reared on those eggs. Such an effect has been modeled in ecological theory as a “bottom up cascade.” Improved knowledge of the nutritional ecology of parasitoids and hosts can lead to improved understanding of the ecological mechanisms affecting host plant, host, and parasitoid abundance, as well as to improved efficiency and quality of Trichogramma production in mass rearing programs.

HPLC sugar analysis reveals the nutritional state and the feeding history of parasitoids

Summary Adult parasitoids depend on sugar‐rich foods such as nectar and honeydew to meet their energy requirements. Many laboratory studies have established fitness benefits of sugar feeding for parasitoids. Nevertheless, we know little about the nutritional ecology of parasitoids in the field, chiefly because of the limited specificity of methods applicable for field studies. Here we use high‐performance liquid chromatography (HPLC) analysis to study the sugar profile of Cotesia glomerata L. and Microplitis mediator Haliday relative to feeding‐treatment. We identify the overall sugar level and the ratio of glucose to fructose as two parameters that in combination unambiguously characterize an individual's nutritional state and feeding history. Unfed parasitoids contained low total sugar levels and glucose levels that typically exceeded fructose levels more than five‐fold. Parasitoids with constant access to sucrose had high overall sugar levels with a balanced glucose–fructose ratio. The marked shift of the glucose–fructose ratio after feeding was still evident in C. glomerata individuals whose total sugar content had decreased to unfed levels after 3 days of starvation. This makes it possible to distinguish between unfed individuals and those that did feed several days ago. In addition to revealing past feeding events, HPLC analysis also enables the identification and quantification of a wide spectrum of sugars present in each specimen. When food sources contain specific sugars this can provide additional information about the type of sugar source consumed. HPLC analyses revealed that trehalose, considered to be the ‘insect haemolymph sugar’, is not present in the two species investigated here. Overall, HPLC sugar analysis provides a powerful tool to investigate energy status, feeding history and nutritional physiology of field‐collected parasitoids.

Discovery of insect parasitism and subsequent development of parasitoid research in Japan

Abstract In Japan, early research on insect parasitism, i.e., from 1850 onwards, had a profound effect of sericulture. Insect parasitism in Japan was recognized in 1856, when S. Iimuro first described parasitism of silkworm larvae by the tachinid Blepharipa sericariae. C. Sasaki published a full report on the life history of this parasitic fly in 1887, showing that the female fly laid microtype eggs on mulberry foliage, that these eggs were ingested by the silkworm larva as it fed, and that they hatched in the host gut to parasitize it. C. Sasaki shared credit for this epoch-making discovery with his father, N. Sasaki, who pioneered research on parasitism in Japan. Much work on ecology, behavior, physiology, and control of this pest fly was done from the time of discovery until the 1950s, when sericulture began to decline in Japan. Subsequent contributions to parasitoid research included Utida’s [Ecology 38 (1957) 442] outstanding work on population interactions in laboratory host–parasitoid systems. More recently, most parasitoid research has dealt with ecology, especially behavioral ecology of parasitoids and the use of parasitoids in biological control of insect pests. However, the taxonomy of the parasitoid fauna is not well developed in Japan, constituting a major obstacle to continued ecological research.

Gut sugar analysis in field-caught parasitoids: Adapting methods originally developed for biting flies

The ability to determine the presence and identity of sugars in the guts of adult parasitoids in the field would aid researchers in addressing long-standing problems in parasitoid ecology. Until very recently, however, gut sugar analyses have not been carried out on parasitoids. This is despite the development and use of methodologies for gut sugar analyses in biting flies (mosquitoes, sand-flies, black-flies, horse- and deer-flies, and biting midges) for decades. Methods used have been the cold anthrone test for the detection of gut sugars, and various forms of chromatography for the identification of gut sugars. We review the use of these methods in biting fly research and then describe the nascent field of gut sugar analyses in parasitoids. Both cold anthrone and chromatography tests have begun to be used on field-caught parasitoids, and we describe progress from our own work. We used cold anthrone on the aphid parasitoid Aphelinus albipodus (Hymenoptera: Aphelinidae), and results from one field study show that approximately one-fifth of individuals tested were positive for gut sugars. The characteristics of the field site point to the primary source of these gut sugars as being aphid honeydew. We also analysed the gut contents of Diadegma insulare (Hymenoptera: Ichneumonidae), a parasitoid of diamondback moth. In this case, HPLC analyses showed that over 85% of field-captured individuals had fed upon sugars. These same analyses suggested that honeydew may have been a major source of the gut sugars in this case also, but the sugar profiles suggest some nectar feeding. Understanding the importance of various sugar sources on parasitoid activity and effectiveness will facilitate the incorporation of sugar sources in habitat manipulation programmes as a part of IPM.

Effects of plant quality on the population ecology of parasitoids

Effects of plant quality on the population ecology of parasitoids

Marking Behavior and Discrimination of Concealed Hosts by the Ectoparasitoid, Dinarmus basalis Rond. (Hym. Pteromalidae)

The parasitoid species, Dinarmus basalis, attacks bruchid beetle larvae concealed within hard seeds. Female wasps are able to discriminate the quality of their host but the position in the concealed host system where this discrimination takes place remains unclear. Under laboratory conditions, we investigated whether the cues were detectable: (1) at a medium or short distance from the seed, (2) on the seed, or (3) within the seed, at the point of contact with the host. In particular, we investigated whether internal or external markings are applied by the parasitoid and then recognized in a subsequent encounter or by a conspecific encountering the host. Detailed behavioral observations did not provide evidence of markings being applied onto the seed or used, but showed that host discrimination occurred on the basis of internal cues. The lack of evidence of external markings is unexpected and raises the question as to which circumstances in the parasitoid's ecology and life history could result in such a lack not causing a reduction of fitness.