Host-parasitoid Relationships Research Articles

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.

The genome of the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera, Scelionidae), a model organism and biocontrol agent of stink bugs

Trissolcus basalis (Wollaston) is a minute parasitic wasp that develops in the eggs of stink bugs. Over the past 30 years, Tr. basalis has become a model organism for studying host finding, patch defense behavior, and chemical ecology. As an entry point to better understand the molecular basis of these factors, in addition to filling a critical gap in the genomic resources available for parasitic Hymenoptera, we sequenced and assembled the genome of Tr. basalis using short (454, Illumina) and long read (Oxford Nanopore) sequencing technologies. The three sequencing methods produced 32 million reads (4.10 Gb; 27.9×), which were assembled into 7,586 scaffolds. The 147 Mb (N50: 42.8 kb) assembly contains complete sequences for 93.1% of the insect BUSCO dataset, and an extensive annotation protocol resulted in 14,158 protein-coding gene models, 12,197 (86%) of which had a blast hit in GenBank. Repetitive elements comprised 13.8% of the genome, and a phylogenomic analysis recovered Tr. basalis as sister to Chalcidoidea, a result in line with other studies. We identified 174 rapidly evolving gene families in Tr. basalis, including olfactory receptors and pheromone/general odorant binding proteins. These genetic elements are an obligatory portion of the parasitoid-host relationship, and the draft genome of Tr. basalis has and will continue to be useful in elucidating these relationships at finer resolution.

The larval saliva of an endoparasitic wasp, Pteromalus puparum, suppresses host immunity

In the lengthy co-evolution between insects and their animal or plant hosts, insects have evolved a wide range of salivary strategies to help evade host defenses. Although there is a very large literature on saliva of herbivorous and hematophagous insects, little attention has been focused on the saliva of parasitoid wasps. Some parasitoid species are natural enemies that effectively regulate insect population sizes in nature that they are applied for biological control of agricultural pests. Here, we demonstrate the influence of the endoparasitoid, Pteromalus puparum, larval saliva on the cellular and humoral immunity of its host. Larval saliva increases mortality of hemocytes, and inhibits hemocyte spreading, a specific cellular immune action. We report that high saliva concentrations inhibit host cellular encapsulation of foreign invaders. The larval saliva also inhibits melanization in host hemolymph. The saliva inhibits the growth of some bacterial species, Bacillus subtilis, Staphylococcus aureus and Pseudomonas aeruginosa in vitro. This may promote larvae fitness by protecting them from infections. Insight into such functions of parasitic wasp saliva provides a new insight into host-parasitoid relationships and possibly leads to new agricultural pest management technologies.

Parasitoids of Drosophilids in the Brazilian Savanna: Spatial-temporal Distribution and Host Associations with Native and Exotic Species.

Host-parasitoid interactions may have a relevant role not only in ecological processes but also in human procedures such as biological control and the management of invasive species. Although the Drosophila-parasitoid system has been widely used for investigating all aspects of host-parasitoid relationships, it is still poorly understood in tropical areas. Here, we investigate the richness, spatial-temporal distribution, and host associations of parasitoids attacking drosophilid flies in the core region of the Brazilian Savanna, a hotspot of biodiversity. Using different methods, we collected wasps on several occasions over 7years and found 13 species representing families associated with drosophilid larvae (Figitidae, Braconidae) and pupae (Pteromalidae, Eurytomidae, Dipriidae). The dominant species infesting larvae and pupae were Dicerataspis grenadensis Ashmead and Pachycrepoideus vindemmiae (Rondani), respectively. Spalangia simplex Perkins was recorded for the first time in the Brazilian Savanna. Although our study was not designed to evaluate collection methods, we observed that they captured different subsets of the wasp community. The spatiotemporal distribution of wasps followed those of drosophilids: they were more abundant in forests and during the rainy season, suggesting that the abundance of hosts, especially native drosophilids, is an important factor determining the assemblage structure and population dynamics of parasitoids. Common parasitoids and drosophilids were associated with more than one host/antagonist species, suggesting that caution should be used for the selection of biological control agents. This study confirms the role and relevance of natural vegetation in preserving biodiversity and ecosystem services, especially in a biome severely threatened by agricultural expansion.

New records and a voucher collection of parasitoid wasps (Hymenoptera) inhabiting agroforestry systems in the colombian amazon basin

Cacao (Theobroma cacao) and copoazú (T. grandiflorum) agroecosystems represent a common source of income or many small-scale farmers in the Colombian Amazon basin. Most of these systems are set in low disturbance environments; they are considered biodiversity-friendly ecosystems inhabited by several groups of insects. In this study, we carried out a preliminary taxonomic inventory of the microhymenopteran parasitoids present in these agroforestry systems. Twenty-six localities of the Amazonian basin of Colombia were sampled using several insect collecting methods (Malaise trap, sweep net, pitfall, and rearing boxes). Collected specimens were curated and cataloged, establishing the first taxonomic voucher collection of parasitoids from the Colombian Amazon basin. We identified 767 specimens representing 64 species, 274 morphospecies, 143 genera and 20 families, 34 genera and 16 species of these being recorded for the first time in the country. The genus Gbelcia is reported for the first time from the Neotropical region. A new parasitoid-host relationship was found for Horismenus cupreus (Eulophidae) attacking larvae of Phyllocnistis sp. (Lepidoptera, Gracillariidae), which feeds on Annona montana (Annonaceae) leaves.

Study of aphid parasitoids (Hymenoptera: Braconidae) in Australian grain production landscapes

AbstractAphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) were surveyed within grain production landscapes in Victoria, Australia, between 2017 and 2018, as well as more sporadically nationwide between 2016 and 2019. In addition, Aphidiinae records were collated from insect depositories around Australia and online databases. The 5525 specimens recorded constituted a total of 23 species and seven genera. Diaeretiella rapae (M'Intosh) was the most common species, representing more than 70% of all Aphidiinae recorded. This species also showed a greater northerly geographical range than other Aphidiinae. During sampling between 2017 and 2019, Aphidiinae were reared from mummies to ascertain host–parasitoid relationships. Diaeretiella rapae was again the most commonly reared parasitoid, although parasitoid preference varied with aphid host and between states and territories. An illustrated dichotomous key to Australian Aphidiinae in grain production landscapes is provided for the 11 species sampled in our field surveys. This is the first comprehensive review of Aphidiinae sampled within Australia in over two decades. Knowledge about the diversity and distribution of these parasitoids is important for understanding their impact on current and future invasions of aphid species. In addition, understanding the interactions between grain aphids and their associated parasitoids will further support the inclusion of parasitoid wasps into integrated pest management (IPM) strategies.

Review of Venoms of Non-Polydnavirus Carrying Ichneumonoid Wasps.

Simple SummaryParasitoid wasps play an important role in all terrestrial ecosystems (both natural and agricultural) regulating the population densities of many herbivorous insects. Venom components have been studied in a number of exemplar species, both from a pure science perspective and because of their potential as lead structures for novel insecticides. The Ichneumonoidea comprises some 40,000 described species and several times more undescribed ones. We review the chemistry and physiological actions of these wasp venoms. Only those species that lack genome-encoded polydnaviruses are considered because of the complexity of interactions between venom and polydnavirus. Examples include ecto- and endoparasitoids, and idiobionts (host development arrested at time of parasitisation) and koinobionts (hosts allowed to continue developing). Most associations are with Lepidoptera. Unlike aculeate (stinging) wasps, bees and ants, venoms are dominated by proteins with only a few containing small peptides or biogenic amines. Venom effects include temporary, permanent or no host paralysis, host castration, immune suppression and modifying host metabolism. Few venom components have clearly identified effects. Studied venoms involve only a very small number of ichneumonoid subfamilies outside of those producing polydnaviruses. Suggestions are made regarding other systems that may be worthwhile investigating.Parasitoids are predominantly insects that develop as larvae on or inside their host, also usually another insect, ultimately killing it after various periods of parasitism when both parasitoid larva and host are alive. The very large wasp superfamily Ichneumonoidea is composed of parasitoids of other insects and comprises a minimum of 100,000 species. The superfamily is dominated by two similarly sized families, Braconidae and Ichneumonidae, which are collectively divided into approximately 80 subfamilies. Of these, six have been shown to release DNA-containing virus-like particles, encoded within the wasp genome, classified in the virus family Polydnaviridae. Polydnaviruses infect and have profound effects on host physiology in conjunction with various venom and ovarial secretions, and have attracted an immense amount of research interest. Physiological interactions between the remaining ichneumonoids and their hosts result from adult venom gland secretions and in some cases, ovarian or larval secretions. Here we review the literature on the relatively few studies on the effects and chemistry of these ichneumonoid venoms and make suggestions for interesting future research areas. In particular, we highlight relatively or potentially easily culturable systems with features largely lacking in currently studied systems and whose study may lead to new insights into the roles of venom chemistry in host-parasitoid relationships as well as their evolution.

Deployment of Aggregation-Sex Pheromones of Longhorned Beetles (Coleoptera: Cerambycidae) Facilitates the Discovery and Identification of their Parasitoids.

Longhorned beetles (Coleoptera: Cerambycidae) include many species that are among the most damaging pests of managed and natural forest ecosystems worldwide. Many species of cerambycids use volatile chemical signals (i.e., pheromones) to locate mates. Pheromones are often used by natural enemies, including parasitoids, to locate hosts and therefore can be useful tools for identifying host-parasitoid relationships. In two field experiments, we baited linear transects of sticky traps with pheromones of cerambycid beetles in the subfamily Cerambycinae. Enantiomeric mixtures of four linear alkanes or four linear alkanes and a ketol were tested separately to evaluate their attractiveness to hymenopteran parasitoids. We hypothesized that parasitoids would be attracted to these pheromones. Significant treatment effects were found for 10 species of parasitoids. Notably, Wroughtonia ligator (Say) (Hymenoptera: Braconidae) was attracted to syn-hexanediols, the pheromone constituents of its host, Neoclytus acuminatus acuminatus (F.) (Coleoptera: Cerambycidae). Location and time of sampling also significantly affected responses for multiple species of parasitoids. These findings contribute to the basic understanding of cues that parasitoids use to locate hosts and suggest that pheromones can be used to hypothesize host relationships between some species of cerambycids and their parasitoids. Future work should evaluate response by known species of parasitoids to the complete blends of pheromones used by the cerambycids they attack, as well as other odors that are associated with host trees of cerambycids.

Performance of Ooencyrtus kuvanae (Hymenoptera: Encyrtidae) on two host species, Halyomorpha halys and Philosamia ricini

AbstractThe brown marmorated stink bug, Halyomorpha halys, is an invasive agricultural pest of fruit trees and vegetables. Egg parasitoids play a key role in the reducing of H. halys populations. Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) can parasitize H. halys and complete its life cycle in this host species. Many factors can influence this parasitoid–host relationship. Of these factors, we evaluated the effect of female age, exposure time, and host species on the biological characteristics and fecundity of O. kuvanae reared on eggs of H. halys as well as another previously known host Philosamia ricini (Lepidoptera: Saturniidae). In this study, we used a 3‐year‐old laboratory colony of O. kuvanae. Parasitism rates positively affected by exposure time in P. ricini. The highest parasitism rates were obtained in 5‐ and 7‐day‐old females of both hosts. The highest emergence rates were recorded on P. ricini for 5‐ and 7‐day‐old female P. ricini (81.8% and 84.8%, respectively). The development time of O. kuvanae ranged from 18.4 to 19.1 days on H. halys and 17.7 to 18.3 days on P. ricini. The longevity of O. kuvanae that were provided honey was 38.5 and 47.8 days on H. halys and P. ricini, respectively. The longevity of O. kuvanae that were not provided honey was 2.3 and 2.8 days on H. halys and P. ricini, respectively. The sex ratio was male‐biased (36.5% female) on H. halys and female‐biased (55.2% female) on P. ricini. Fecundity of O. kuvanae was 37.7 and 59.6 progeny per female for H. halys and P. ricini, respectively. The performance of O. kuvanae was lower when compared with its performance on the host P. ricini. Our results suggest that O. kuvanae has potential as new biological control agent for H. halys.

Spatial scale, neighbouring plants and variation in plant volatiles interactively determine the strength of host–parasitoid relationships

Species‐specific responses to the environment can moderate the strength of interactions between plants, herbivores and parasitoids. However, the ways in which characteristics of plants, such as genotypic variation in herbivore induced volatiles (HIPVs) that attract parasitoids, affect trophic interactions in different contexts of plant patch size and plant neighbourhood is not well understood. We conducted a factorial field experiment with white cabbage Brassica oleracea accessions that differ in the attractiveness of their HIPVs for parasitoids, in the context of different patch sizes and presence or absence of surrounding Brassica nigra plants. Parasitism rates of experimentally introduced Pieris brassicae caterpillars and the presence of naturally occurring Pieris spp. caterpillars in the plots were assessed throughout the growing season. The abundance of Pieris caterpillars was neither affected by cabbage accession nor plot size. Later in the season, when B. nigra plants had senesced, fewer caterpillars were found on cabbage plants in plots with a B. nigra border. Parasitism rates fluctuated over the season, and were not affected by plot size. However, the B. nigra border negatively affected parasitism rates on the accession that is less attractive to the parasitoid Cotesia glomerata, but not on the more attractive accession. Our results show that plant variation in HIPVs can differentially influence herbivores and parasitoids depending on characteristics of the surrounding vegetation context. These findings underscore the importance of considering the interaction between focal plant traits and neighbourhood context to reliably predict trophic cascades.

Surveys of stink bug egg parasitism in Asia, Europe and North America, morphological taxonomy, and molecular analysis reveal the Holarctic distribution of Acroclisoides sinicus (Huang & Liao) (Hymenoptera, Pteromalidae)

Halyomorpha halysis an invasive, widespread stink bug for which only short-term solutions are currently available for pest control worldwide. The need for long-term management solutions forH. halyshas driven studies on augmentative and classical biological control of this species, especially by its egg parasitoids. Numerous investigations in Asia, USA, and Europe on native and exotic egg parasitoids ofH. halys, and the effects on non-target pentatomids, have improved the global knowledge of parasitoid-host relationships, uncovered new associations, and led to the discovery of new species. This trend continues withAcroclisoides sinicus, a pteromalid that was described in the 1980’s from Asia. In this work we report recent findings of this species in North America and Europe. Moreover, we propose thatAcroclisoides solussyn. nov., a species described originally from the USA, is conspecific withA. sinicusbased on morphological and molecular analysis.

Tachinid flies (Diptera: Tachinidae) associated with crop pests in northern Cameroon, with the description of a new species of Carcelia Robineau-Desvoidy

SummaryAgroecological research was carried out in northern Cameroon from 2008 to 2014 to develop a strategy aiming to encourage the action of natural enemies against lepidopteran pests in cotton crops and in surrounding landscapes. Tachinidae is one of the most diverse families of Diptera in the Afrotropics and represents an important group of endoparasitoids, although their role as biocontrol agents in crops is still poorly understood in Africa. Tachinid flies were collected and reared from lepidopteran caterpillars found in agricultural settings, with a particular attention to the cotton bollworm, a major pest in the region, and from the coreid Anoplocnemis curvipes. A total of 127 specimens of tachinids belonging to 21 species/morphospecies have been recorded, including a new species of Carcelia, Carcelia ethillamima Cerretti, n. sp. and six new records for Cameroon, Campylocheta risbeci, Goniophthalmus halli, Pseudogonia rufifrons, Carcelia peraequalis, Exorista xanthaspis, and Paraclara magnifica. The study improves our knowledge of these parasitoids in Central Africa and our understanding of host–parasitoid relationships in this dipteran family.

Background noise disrupts host-parasitoid interactions.

The soundscape serves as a backdrop for acoustic signals dispatched within and among species, spanning mate attraction to parasite host detection. Elevated background sound levels from human-made and natural sources may interfere with the reception of acoustic signals and alter species interactions and whole ecological communities. We investigated whether background noise influences the ability of the obligate parasitoid Ormia ochracea to locate its host, the variable field cricket (Gryllus lineaticeps). As O. ochracea use auditory cues to locate their hosts, we hypothesized that higher background noise levels would mask or distract flies from cricket calls and result in a decreased ability to detect and navigate to hosts. We used a field manipulation where fly traps baited with playback of male cricket advertisement calls were exposed to a gradient of experimental traffic and ocean surf noise. We found that increases in noise amplitude caused a significant decline in O. ochracea caught, suggesting that background noise can influence parasitoid–host interactions and potentially benefit hosts. As human-caused sensory pollution increases globally, soundscapes may influence the evolution of tightly co-evolved host–parasitoid relationships. Future work should investigate whether female cricket phonotaxis towards males is similarly affected by noise levels.

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.

Life History and Distributional Information for Three Species of Periploca Braun, 1919 (Lepidoptera: Cosmopterigidae) Inhabiting Juniperus spp. (Cupressaceae) Berries in the Western U.S.

Expansion of native junipers, Juniperus Linnaeus (Cupressaceae), is altering landscapes in the western U.S., prompting extensive management efforts to counter this spread and the negative effects on impacted ecosystems. Our studies investigating sources of seed mortality in western juniper, Juniperus occidentalis Hooker; Utah juniper, Juniperus osteosperma (Torrey) Little); and California juniper, Juniperus californica Carriere, have revealed a number of previously unreported seed-attacking arthropods. One of the most commonly encountered insects at collection sites in California and Nevada are cone-boring cosmet moths (Cosmopterigidae) in the genus Periploca Braun, 1919. DNA analysis of insect adults and immatures both reared and dissected from juniper berries definitively associated Periploca adults with their immature stages and with seed damage while also screening for parasitoid DNA to reveal parasitoid-host relationships. Sequence data for Periploca adults and larvae revealed the presence of three species of Periploca attacking juniper berries at our survey locations. These have been identified as P. atrataHodges, 1962, commonly referred to as the juniper cone moth, along with P. juniperiHodges, 1978, and P. serrulataHodges, 1978. Previously unreported details regarding the life histories of these three species of Periploca, all of which were encountered in western, Utah, and California juniper, were revealed. In addition, berry dissections, rearing efforts, and DNA sequence data have linked numerous parasitoids to juniper berry-infesting Periploca. These findings develop a more refined understanding of the genus Periploca and the arthropod community infiuencing juniper seed production, which can provide potentially valuable tools for the ongoing management of juniper expansion.

Environmental thermal levels affect the phenological relationships between the chestnut gall wasp and its parasitoids

AbstractStudies of thermal level‐related asynchrony in a host–parasitoid relationship are necessary to understand the effects of climate change on new host–parasitoid interactions. In the Asian chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae) and its Chalcidoidea parasitoids, phenological synchrony is assumed to be weather‐dependent in a new area of expansion. To evaluate the effects of environmental thermal regimes on the host, a phenology model for different cynipid stages (larvae, pupae, adults, and adult emergence) and a host–parasitoid phenological estimator are developed in three chestnut fields during two successive growth seasons and subsequently validated in areas with chestnut fields at two different altitudes. Comparisons of the timings of the juvenile and adult stages with those of the parasitoid complex demonstrate that the shortest period of occurrence for cynipids within galls has negative effects on the host–parasitoid relationships at higher temperature levels, thereby increasing phenological asynchrony for some parasitoids species. Reducing the development time of pupae and adults decreases the likelihood of success for some parasitoid species at higher temperature levels. We also record the extension of the gall wasp development time (approximately 15 days) at higher altitudes (linked to a lower mean temperature of approximately 1.5 °C). These results highlight how parasitization on the new hosts is dependent on the host phenology and, in the present study, is limited by the short duration of the presence of the host in galls, which could explain the considerable differences in cynipid gall wasp parasitization recorded at different altimeters.

New invasive bruchine species (Chrysomelidae: Bruchinae) in the fauna of Romania, with a review on their distribution and biology

SummaryFour allochthonous seed beetles, associated with Gleditsia triacanthos L., Albizia julibrissin Durraz. and Cercis siliquastrum L., are reported from Romania for the first time. They are Megabruchidius dorsalis (Fåhraeus, 1839), M. tonkineus (Pic, 1914), Bruchidius terrenus (Sharp, 1886) and B. siliquastri Delobel, 2007 respectively. Their distribution (native, in Europe and Romania) is reviewed. Notes on biology are provided and morphological characters for the identification of these species are discussed. We also provide information about the parasitoid assemblages associated with these seed beetles, three of the parasitoid–host relationships being reported here for the first time.

Thermal plasticity potentially mediates the interaction between host Chilo partellus Swinhoe (Lepidoptera: Crambidae) and endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae) in rapidly changing environments.

Increasing climatic average temperatures and variability elicit various insect physiological responses that affect fitness and survival and may influence subsequent trophic interactions in agroecosystems. In this background, we investigated short- and long-term plastic responses to temperature of the laboratory-reared stemborer Chilo partellus and its larval endoparasitoid Cotesia flavipes. Rapid cold- and heat-hardening effects in C. partellus larvae, pupae and adults and C. flavipes adults were highly significant (P < 0.001). High-temperature acclimation improved critical thermal limits and heat knockdown time in C. partellus larvae and C. flavipes adults, respectively. Low-temperature acclimation enhanced the supercooling point in C. flavipes and the chill coma recovery time in both C. partellus larvae and C. flavipes adults. The results of this study suggest that thermal plasticity may enhance the survival of these two species when they are subjected to lethal low and high temperatures. However, C. partellus appeared to be more plastic than C. flavipes. These results have three major implications: (1) C. partellus may inhabit slightly warmer environments than C. flavipes, suggesting a potential mismatch in biogeography; (2) host-parasitoid relationships are complex and are probably trait dependent, and (3) host-parasitoid differential thermal plastic responses may offset biocontrol efficacy. These results may help inform biocontrol decision making under conditions of global change. © 2017 Society of Chemical Industry.

High nymphal host density and mortality negatively impact parasitoid complex during an insect herbivore outbreak.

Insect herbivore outbreaks frequently occur and this may be due to factors that restrict top-down control by parasitoids, for example, host-parasitoid asynchrony, hyperparasitization, resource limitation and climate. Few studies have examined host-parasitoid density relationships during an insect herbivore outbreak in a natural ecosystem with diverse parasitoids. We studied parasitization patterns of Cardiaspina psyllids during an outbreak in a Eucalyptus woodland. First, we established the trophic roles of the parasitoids through a species-specific multiplex PCR approach on mummies from which parasitoids emerged. Then, we assessed host-parasitoid density relationships across three spatial scales (leaf, tree and site) over one year. We detected four endoparasitoid species of the family Encyrtidae (Hymenoptera); two primary parasitoid and one heteronomous hyperparasitoid Psyllaephagus species (the latter with female development as a primary parasitoid and male development as a hyperparasitoid), and the hyperparasitoid Coccidoctonus psyllae. Parasitoid development was host-synchronized, although synchrony between sites appeared constrained during winter (due to temperature differences). Parasitization was predominantly driven by one primary parasitoid species and was mostly inversely host-density dependent across the spatial scales. Hyperparasitization by C. psyllae was psyllid-density dependent at the site scale, however, this only impacted the rarer primary parasitoid. High larval parasitoid mortality due to density-dependent nymphal psyllid mortality (a consequence of resource limitation) compounded by a summer heat wave was incorporated in the assessment and resulted in density independence of host-parasitoid relationships. As such, high larval parasitoid mortality during insect herbivore outbreaks may contribute to the absence of host density-dependent parasitization during outbreak events.

Life cycles and host–parasitoid relationships of five species of Leucospis wasps in Argentina (Hymenoptera: Leucospidae)

ABSTRACTThe genus Leucospis Fabricius is comprised of parasitoid wasps relatively uncommon in nature. Their immature stages develop on aculeate Hymenoptera, in particular solitary bees, but hosts are known for only around 25 Leucospis species (about 20% of 115–120 world species), so the true relationship of this family with bees is largely unknown. Here we report on individuals of five species of Leucospis wasps which emerged from nests of different bee and wasp species during distinct sampling periods during a trap-nesting programme, in two contrasting areas: agro-ecosystems and natural habitats in the Pampean region. Some of these nests were parasitised by L. cayennensis Westwood, L. coxalis Kirby, L. egaia Walker, L. pulchriceps Cameron and L. signifera Bouček. Our results expand the available information of host species for L. cayennensis, L. coxalis, L. egaia and L. pulchriceps and represent the first record of hosts associated with L. signifera. The hosts were only bee species of the genera Centris, Tetrapedia (family Apidae) and Megachile (Megachilidae). These species were more abundant in the natural reserve than in agro-ecosystems, suggesting that anthropogenic activities could negatively affect their populations. Most nests were attacked in one (43.7%) or two (40.7%) cells, but the remaining nests (16.5%) had more (up to seven cells). However, the position of the attacked cells was variable, suggesting that females of Leucospis species oviposit in recently built cells, and that the hatching of larvae is delayed, or that the first larval stage waits until the host larva reaches a sufficient size to attack.