Field evidence that host selection by conopid parasitoids is related to host body size

Summary The body size of the host insect in which a parasitoid develops can have important effects on its development and life history. Large and small host body size have both been suggested to be advantageous to parasitoids, depending on the life-history of the species concerned. We test field data on the bumblebeeBombus terrestris and its conopid parasitoids for evidence of differences in size between parasitised and unparasitised worker bees. Bees acting as hosts for conopid parasitoids are on average larger-bodied than unparasitised bees. This result holds for bees collected in two different years, and whether bees are collected while foraging or from the nest. The results we present demonstrate differential parasitism of hosts of different body sizes, but do not necessarily indicate active host choice by conopids. However, they are in agreement with independent evidence that conopids develop more successfully in large-than in small-bodied hosts.     

Relationships between parasitism,bumblebee foraging behaviour,and pollination service to Trifolium pratense flowers

1. Parasite effects on host behaviour frequently alter their hosts' trophic interactions. There are many compelling examples of such effects in herbivore‐based trophic interactions, but less attention has been paid to how parasite effects on host behaviour can alter mutualistic interactions. 2. Pollination mutualisms depend greatly on pollinator behaviour, and many pollinators are attacked by a wide range of parasites and parasitoids. 3. To investigate whether parasites affect pollination service via changes in host behaviour, natural variation in conopid fly parasitism was used to investigate the relationship between infection and Bombus impatiens Cresson behaviour foraging on arrays of Trifolium pretense L. flowers in the laboratory. The consequences of infection for seed set and seed mass were also examined. 4. Conopid parasitism was not related to any measured behavioural response; however, flowers visited by conopid‐parasitised bees set significantly heavier seeds than those visited by unparasitised bees. Larger bees were more likely to be parasitised, but the relationship between parasitism and seed set still held after accounting for body size. 5. The present results demonstrate that parasitoids may have positive impacts on per‐visit pollination, but, because larger bees were more frequently parasitised, parasitism could also affect pollination by removing the largest pollinators from the population.     

Fluctuating asymmetry, call structure and the risk of attack from phonotactic parasitoids in the bushcricket Sciarasaga quadrata (Orthoptera: Tettigoniidae)

The acoustically orienting parasitoid Homotrixa alleni (Diptera: Tachinidae) is a significant mortality factor of calling male Sciarasaga quadrata (Orthoptera: Tettigoniidae), with less than 10% of males escaping parasitism within the duration of the calling season. This study examined fluctuating asymmetry (FA) (small, random deviations from perfect symmetry) in five morphological traits in S. quadrata and its relation to the survival of calling males in the field. A significant relationship was demonstrated in only a single trait; across three consecutive field seasons and among each of the collections per season, parasitised males were shown to have significantly more asymmetric hind tibia than unparasitised males. Since the morphological development of males is complete prior to parasitoid attack, this relationship is not caused by the activities of the parasitoid. Further experimentation revealed that there was no relationship between the level of FA in the hind tibia and the success of parasitism, with males artificially parasitised in the laboratory showing no difference in FA from those where parasitism was unsuccessful. Instead, FA was shown to be negatively related to chirp length, an aspect of call structure that significantly affects the survival of calling males under parasitism risk in the field. We explore the possible reasons why more asymmetric males produce calls of shorter chirp length and hypothesise that the difference in hind tibia asymmetry seen between parasitised and unparasitised males in the field is related to host location in H. alleni rather than the inability of S. quadrata to defend itself against parasitoid attack. Received: 14 November 1997 / Accepted: 20 April 1998     

Patterns of parasite infection in bumble bees (Bombus spp.) of Northern Virginia

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Patterns of parasitism among conopid flies parasitizing bumblebees

The effects of host size and host species on the prevalence and fitness of conopid flies (Diptera: Conopidae) parasitizing bumblebees (Hymenoptera: Apidae) were investigated. Field data from nine sites across south‐western Alberta, Canada, showed that conopids parasitized, on average, 12.3% of workers and 3.5% of male bees. In general, bee mass was a better predictor of host use and conopid offspring size than bee species. Host mass could not, however, explain the very low prevalence of conopids in the long‐tongued bumblebee, Bombus californicus Smith, or in male bees in general. Conopids predominately infested bees of intermediate size, and as a result, occurred most commonly in the intermediately sized species, B. flavifrons Cresson. Host quality, in terms of conopid offspring size, increased as a non‐linear function of bee size. The results are discussed with respect to the impact of conopids on bumblebee populations, and the relation between host quality and patterns of host use.     

A new threat to honey bees, the parasitic phorid fly Apocephalus borealis

Honey bee colonies are subject to numerous pathogens and parasites. Interaction among multiple pathogens and parasites is the proposed cause for Colony Collapse Disorder (CCD), a syndrome characterized by worker bees abandoning their hive. Here we provide the first documentation that the phorid fly Apocephalus borealis, previously known to parasitize bumble bees, also infects and eventually kills honey bees and may pose an emerging threat to North American apiculture. Parasitized honey bees show hive abandonment behavior, leaving their hives at night and dying shortly thereafter. On average, seven days later up to 13 phorid larvae emerge from each dead bee and pupate away from the bee. Using DNA barcoding, we confirmed that phorids that emerged from honey bees and bumble bees were the same species. Microarray analyses of honey bees from infected hives revealed that these bees are often infected with deformed wing virus and Nosema ceranae. Larvae and adult phorids also tested positive for these pathogens, implicating the fly as a potential vector or reservoir of these honey bee pathogens. Phorid parasitism may affect hive viability since 77% of sites sampled in the San Francisco Bay Area were infected by the fly and microarray analyses detected phorids in commercial hives in South Dakota and California's Central Valley. Understanding details of phorid infection may shed light on similar hive abandonment behaviors seen in CCD.     

Nesting aggregation as a predictor of brood parasitism in mason bees (Osmia spp.)

1. Parasitism can be an important source of mortality for insect populations; however, we know little about the factors influencing vulnerability of wild bees to parasites. Mason bees (genus Osmia; Hymenoptera: Megachilidae) are important pollinators of crops and wild plants and are vulnerable to attack by brood parasites. High nest densities may increase rates of brood parasitism by attracting disproportionate numbers of parasites. 2. Three years of field observations from multiple sites were analysed to assess whether mason bee brood parasitism increased with host density. Mason bees were allowed to nest in artificial nesting blocks and establish natural variation in nesting density. Nest cells constructed by bees were checked for the presence of parasite eggs. 3. Parasitism of nest cells strongly increased with the number of actively nesting bees at a nesting block. Mason bees showed no preference for nesting in blocks that were occupied or unoccupied by other mason bees. Parasitism also increased with the number of days a nest was provisioned and decreased over the course of the season. Nest cells constructed last in a nest were significantly more parasitised than inner cells, despite being sealed against invasions. 4. These findings show positively density‐dependent parasitism in mason bees. They also suggest that bees terminate parasitised nests, causing parasitised cells to become outermost nest cells – a behaviour that may represent a defence against parasites. Our results have implications for the management of mason bees as agricultural pollinators, as cultivating them at high densities could reduce offspring survival.     

Parasite altered micro-distribution of Gammarus pulex (Crustacea: Amphipoda)

In a river survey, Gammarus pulex amphipods both unparasitised and parasitised with the acanthocephalan Echinorhynchus truttae were distributed similarly with respect to flow regimen, tending to be more abundant in faster, shallower, riffle patches. However, there was a higher prevalence of parasitism in faster, shallower areas than in slower, deeper areas and abundance correlated with macrophyte coverage for unparasitised but not parasitised amphipods, indicating subtle differences in habitat usage. A laboratory 'patch' simulation indicated that parasitism influenced micro-distribution. There were higher proportions of unparasitised amphipods in/under stone substrates and within weed. In contrast, there were higher proportions of parasitised amphipods in the water column and at the water surface. As the experiment progressed, unparasitised but not parasitised amphipod habitat usage shifted from those micro-habitats above the substrate and in the water column to those in/under the substrates. Experiments also demonstrated that parasitised amphipods were more active and had a greater preference for illumination. Previous studies of the effects of acanthocephalan parasitism of amphipod hosts have focussed on how drift behaviour is altered, now we show that subtle differences in micro-habitat usage could translate to greatly increased vulnerability to fish predation. We discuss how aggregation of parasitised individuals within specific habitats could promote parasite transmission.     

Effects of starvation and parasitism on foregut contraction in larval Manduca sexta

Larvae of Manduca sexta are parasitised by the braconid wasp, Cotesia congregata. In this study we examined whether contraction activity of the semi-isolated foregut was affected by parasitism. Parasitised larvae fed significantly less compared with unparasitised control larvae, therefore starved unparasitised animals were used as controls. Rate and force of foregut contraction in control caterpillars significantly increased with days of starvation. However, only contraction force in foreguts of parasitised larvae increased over time following infection. The presence of food in the foregut of caterpillars starved 7 days suggested that food moved anteriorly from the midgut and that contraction became antiperistaltic, but only normal peristalsis occurred in parasitised caterpillars. Rate and force of gut contractions may be controlled independently and starvation did not truly mimic the effects of the parasitoids. Dissection of caterpillars with emerged wasps indicated that 47% had a single wasp larva wedged between the brain and foregut. Removal of this wasp caused an increased rate of foregut contraction of the caterpillar. Brain removal resulted in an increased rate of foregut contraction only for unparasitised insects. Sectioning of the recurrent nerve temporarily eliminated foregut contraction, but the contraction began again in 250 s in parasitised caterpillars prior to wasp emergence, compared with over 500 s for unparasitised controls and parasitised caterpillars following wasp emergence.     

Endoparasitic flies,pollen-collection by bumblebees and a potential host-parasite conflict

Summary Conopid flies (Conopidae, Diptera) are common larval parasites of bumblebees. The larva develops inside the abdomen of workers, queens and males. Development is completed within 10–12 days after oviposition when the host is killed and the parasite pupates in situ. Development results in parasitised bees becoming unable to carry large loads of nectar, as the conopid larvae reside where the honey crop is normally located. Furthermore, an addition to the bee's unloaden body mass is likely (average larval weight reached at pupation by the common parasite species Sicus ferrugineus: ±SD 36.3±12.3 mg, n=59; by Physocephala rufipes: 55.8±16.9 mg, n=108). We here asked whether the propensity of workers of the bumblebee Bombus pascuorum to collect nectar rather than pollen is related to the presence of conopid larvae. For samples of bees (n=2254 workers) collected over 3 years of field studies in northwestern Switzerland, there was no difference in the frequency of bees caught as pollen collectors among parasitised (38.1% of cases, n=210) as compared to non-parastised bees (43.9%, n=360) ( ²=1.83, n.s.). However, compared to the non-parasitised bees (n=360), those hosts containing a third (last) instar larva (n=9) were less likely to collect pollen than expected by chance ²=6.91, P=0.003. Similarly, hosts with short survival time between capture and being killed by the developing larva (which hence must have harboured a late instar parasite at time of capture) were less likely to collect pollen (8%, n=25) than those found not parasitised (37.6%, n=891 ²=9.16, P<0.001). Late instar larvae grow so big that they fill the entire abdomen. Although there was also a tendency for presumably older bees to collect less pollen, this is unlikely to explain the observations. We also discuss whether these changes in foraging behaviour of bumblebees may reflect a host-parasite conflict over the type of resource to be collected.     

Selfing rates in natural populations of Echium vulgare: a combined empirical and model approach

1. We quantified geitonogamous selfing in Echium vulgare , a self-compatible, bumble-bee pollinated plant. A maximum estimate of selfing was determined using a paternity analysis with RAPDs. In the first experiment, bumble-bees visited a sequence of virgin flowers. The percentage selfing increased rapidly from 12% in the first flower visited, up to 50% in the 15th flower visited in the sequence. In the second experiment, when bees visited plants in a natural population, the average selfing of plants increased with the number of open flowers from 0% to maximally 33%.
2. The results obtained in both experiments are consistently lower than predicted by our model on pollen dynamics ( Rademaker, de Jong & Klinkhamer 1997 ). We modified the model on pollen dynamics to link it more to the field situation with observations on flower stage, flower opening and bumble-bee preference, so that the bumble-bees encounter a variable number of pollen grains per flower. We also adjusted the parameters. If less pollen adheres to the bee (25% instead of 50%) after removal from the anthers, or if bees arrive at a plant with more pollen grains (6000 instead of 4448), the predictions of the model in regard to selfing could be improved but were still high compared with the observed selfing rates measured with RAPDs.
3. We suggest that the model is consistent with pollen dynamics in the field. However, post-pollination processes like selective abortion could play a role in E. vulgare .     

Low parasitoid success on a myrmecophilous host is maintained in the absence of ants

Abstract.  1. Studies of Dinocampus coccinellae , a parasitoid of ladybird beetles, have generally shown congruence between field parasitism rates of different host species and parasitoid preference and/or host suitability in the laboratory, suggesting that host intrinsic factors rather than habitat-related extrinsic factors are of greatest importance in determining D. coccinellae occurrence.
2. The myrmecophilous Coccinella magnifica exhibits much lower D. coccinellae prevalence in the field than most other Coccinella species: it has been suggested that this is a manifestation of enemy-free space provided by the predatory Formica rufa group ants with which the C. magnifica occurs.
3. Coccinella magnifica collected at the same time and locality as parasitised Coccinella septempunctata were unparasitised by D. coccinellae . In the laboratory, in the absence of ants, although the parasitoid attacked C. magnifica as readily as C. septempunctata , C. magnifica was not parasitised successfully.
4. Such results are consistent with those from other ladybirds and C. magnifica does not now benefit directly from any putative D. coccinellae -free space provided by aggressive ants. Because its close relatives exhibit high levels of D. coccinellae parasitism, C. magnifica may be useful in determining some elements important in the evolution of host protection against parasitoid attack.     

Factors affecting parasite prevalence among wild bumblebees

1. Bumblebees are important pollinators in North America and are attacked by a range of parasites that impact their fitness; however, few studies have investigated the extent or causes of parasitism in North America. 2. This study used a 2‐year multi‐site survey of bumblebee parasitism to ask: (i) how common are parasitoid conopid flies and the internal parasites Crithidia bombi and Nosema bombi in Massachusetts; and (ii) what factors are correlated with parasitism? 3. Infection rates by all three parasites were higher in this study than previously documented in North America. Overall, conopids infected 0–73% of bees in each sample, C. bombi infected 0–82% of bees, and N. bombi infected 0–32%. 4. Conopid flies infected female bees more than males and intermediate‐sized bees more than large or small bees. Crithidia bombi infection rates were higher in certain bee species and sites, and exhibited a unimodal pattern of prevalence over time. Nosema bombi parasitism was higher in male than female bees. 5. Infection by N. bombi in two rare bumblebee species was higher than expected based on parasitism rates of common bee species but C. bombi infection was lower. If high prevalence of N. bombi in these bumblebee species is common, parasitism may be a potential cause of their decline. 6. Given the documented effects of these parasites, the high levels of infection may affect bee populations in Massachusetts and threaten the stability of their valuable ecosystem services.     

Effect of nest and nest site characteristics on the risk of cuckoo Cuculus canorus parasitism in the great reed warbler Acrocephalus arundinaceus

The risk of cuckoo Cuculus canorus parasitism for great reed warbler Acrocephalus arundinaceus nests was evaluated in respect to nest and nest site structure in the reedbeds along canals in central Hungary, In total 90 nests were analysed, from which 31 remained unparasitised. 37 were single parasitised and 22 multiple parasitised. Multiple discriminant analysis, based on eight structural variables, separated well the unparasitised clutches from the cases of single and multiple parasitism, but the latter two categories also showed a weaker separation. Nests close to cuckoo vantage points are most vulnerable to parasitism. The variable "distance from nest to closest available cuckoo perch site" (tree or electric wire) played the most important role in the risk of parasitism. It showed highly significant differences among the groups: lowest distances were found in the case of multiple parasitism, and the highest distances were measured when nests remained unparasitised. Additionally, "nest visibility" also showed significant differences among the three groups: a more visible nest is more likely to be parasitised. Risk of parasitism affects on the host on two levels: 1) female cuckoos search for nest-building hosts from a perch site, but 2) when they are in the act of parasitism, they can find more visible nests in the reed. Besides the robust effects of the variables "distance to cuckoo perch site" and "nest visibility", the variable "distance from nest to open water" may reduce, but "nest volume" increases the risk of multiple parasitism. Differences between cases of single and multiple parasitism are weak, mainly affected by chance. We explain it by the high abundance of the cuckoo, the parasitism rate was 65.6% (59/90), Cuckoos parasitised almost all of the available nests in the close vicinity of potential perch sites. There was no evidence that great reed warblers nested closer to each other when risk of parasitism was high.     

Parasitism and ant protection alter the survival of the lycaenid Hemiargus isola

Abstract. 1. Although the majority of lycaenid–ant associations is facultative, few studies have documented the protection benefits provided by ants to lycaenids that are tended facultatively (Pierce & Easteal, 1986; Peterson, 1993).
2. Larvae of Hemiargus isola (Lepidoptera: Lycaenidae) feeding on Dalea albiflora are tended facultatively by several species of ant. In 1999 and 2000, the levels of parasitism and the identities of attendant ants were determined for larvae of H. isola . In addition, the presence of ants was manipulated experimentally to determine the efficacy of protection provided by attendant ants to H. isola .
3. Lycaenids were parasitised by a braconid wasp, Cotesia cyaniridis (Riley), and a tachinid fly, Aplomya theclarum (Scudder). In 1999 and 2000, 62 and 65% of larvae were parasitised; the percentage of the population parasitised did not differ significantly between years. In both 1999 and 2000, parasitism by the braconid wasp C. cyaniridis accounted for > 99% of all parasitism events.
4. Four species of ant, Crematogaster sp., Dorymyrmex sp., Forelius sp., and Formica sp., were associated with 88–99% of the tended lycaenids collected in both 1999 and 2000. For both years, there was a single, numerically dominant species associated with >80% of the tended larvae collected, but the identity of this numerically dominant ant differed between years.
5. Experimental exclusion of ants from D. albiflora plants resulted in 78% larval mortality as a result of parasitism, nearly twice that of larvae that were tended by ants on unmanipulated plants.     

Phorid fly(Phoridae: Megaselia halterate) longevity and the disemination of nematodes (Allantonematidae: Howardula husseyi) by parasitised females

The longevity of male and female Megaselia haltherata, 75% of parasitised by the nematode Howardula husseyi, was studied for 16 days at 20- 21.5 OC. A statistical model fitted to the data indicated that parasitism reduced fly longevity significantly; predicted times to 50% mortality were about 6 days shorter for parasitised males, but only 2 days shorter for parasitised females. An investigation of the number of nematode larvae liberated by female flies at intervals throughout the experiment showed that many had been liberated in the first 4 days, and that the rate of release then gradually declined. A statistical model for nematode dissemination rate was used to estimate the mean number of nematodes released at 4-day intervals by surviving flies containing 1–5 adult H. husseyi. Mass release of laboratory-reared parasitised flies on mushroom farms has been suggested as a possible method of boosting the incidence of parasitism in farm fly populations. The results of the present study indicate that if such a measure were taken in spawn-running rooms then the best effect might be attained by releasing the flies in two batches with one release occurring in the middle of each week of the spawn-run.     

The importance of specialist natural enemies for Chrysomela lapponica in pioneering a new host plant

Abstract.  1. The Salicaceae have been suggested as ancestral host plants of Chrysomela species (Coleoptera: Chrysomelidae). In Chrysomela lapponica , some populations are specialised on salicaceous plants, but others have switched to birch. This study aimed to elucidate the significance of natural enemies as possible selective forces for the host plant shift of C. lapponica from willow to birch.
2. Two C. lapponica populations were studied, one specialised on willow Salix borealis in Finland, and another one specialised on birch Betula pubescens in the Czech Republic. Abundances of predators and parasitoids on birches and willows were recorded at both population sites. Furthermore, field and laboratory experiments were conducted.
3. Field data do not support the hypothesis that generalist predators affected the host shift from willow to birch in C. lapponica.
4. Parasitism of C. lapponica (pre)pupae by a specialised phorid fly was significantly stronger in specimens living on willow than in birch-living ones.
5. The predatory syrphid Parasyrphus nigritarsis specialised on Chrysomelinae was only detected on willows. The syrphid preferred to orient towards substrates treated with defensive larval secretion or faeces of the willow-specialised C. lapponica specimens compared with the birch-specialised ones.
6. The data suggest that specialised parasitoids and predators might have been driving forces for C. lapponica to leave willows and to pioneer birches as sites with a lowered risk of predation and parasitism. This hypothesis is discussed with respect to results of earlier studies on the impact of bottom-up effects by the plant.     

The influence of two endoparasitic wasps, <Emphasis Type="Italic">Hyposoter didymator</Emphasis> and <Emphasis Type="Italic">Chelonus inanitus</Emphasis>, on the growth and food consumption of their host larva <Emphasis Type="Italic">Spodoptera littoralis</Emphasis>

The influence of parasitism by Hyposoter didymator (Thunberg; Hymenoptera: Ichneumonidae) and Chelonus inanitus (Linnaeus) (Hymenoptera: Braconidae) on the growth and food consumption of their host Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) was studied in the laboratory. Parasitised larvae consumed significantly less artificial diet than unparasitised ones. Egg parasitisation by C. inanitus affected host larval consumption from the second day after emergence and it was significantly different from that of unparasitised ones. H. didymator, however, started to reduce larval consumption 4 days after parasitisation on the third instar host larvae. The overall reduction achieved by the larval endoparasitoid H. didymator is higher than that caused by the egg-larval endoparasitoid C. inanitus. The final body weight of a parasitised host larva by H. didymator and C. inanitus was only 6.7 and 13.0% of the maximum weight of an unparasitised sixth instar larva respectively. Moreover, parasitised larvae never reached the last instar. Results indicated that parasitised larvae might cause considerable less damage to the host plant than unparasitised ones.     

Parasite transmission and cannibalism in an amphipod (Crustacea)

In its freshwater amphipod host Gammarus duebeni celticus, the microsporidian parasite Pleistophora mulleri showed 23% transmission efficiency when uninfected individuals were fed infected tissue, but 0% transmission by water-borne and coprophagous routes. Cannibalism between unparasitised and parasitised individuals was significantly in favour of the former (37% compared to 0%). In addition, cannibalism between parasitised individuals was significantly higher than between unparasitised individuals (27% compared to 0%). Thus, parasitised individuals were more likely to be cannibalised by both unparasitised and parasitised individuals. We discuss the conflicting selective forces within this host/parasite relationship, the implications of parasite mediated cannibalism for host population structure and the impacts this may have on the wider aquatic community.     

Host choice and fitness correlates for conopid flies parasitising bumblebees

Two parasitoid flies,Physocephala rufipes andSicus ferrugineus (Diptera, Conopidae), and their hosts,Bombus spp., coexist at various locations in northwestern Switzerland. A detailed field study showed that both conopid species use the hostB. pascuorum to a similar degree, while the hostB. terr-luc (a pooled category ofB. terrestris andB. lucorum) is more frequently parasitised than expected byS. ferrugineus. The hostB. lapidarius in turn is exclusively used byP. rufipes. Furthermore, hosts ofB. terr-luc andB. pascuorum parasitised byS. ferrugineus were larger than hosts parasitised byP. rufipes, or than those not parasitised. The findings suggest thatS. ferrugineus selects larger hosts and may displaceP. rufipes. Pupal weight, a predictor of adult body size and parasitoid fecundity, is positively correlated with host size and larger pupae are more likely to emerge, while host species had no effect on the probability of emergence in either conopid species. Host species affected pupal weight inS. ferrugineus, but not inP. rufipes, althoughP. rufipes grew larger in hosts of a given size. Daughters emerged from larger pupae than males, but this did not correlate with larger host sizes. These observations add to the scarce knowledge of dipteran parasitoids.