Temperature affects interaction of visual and vibrational cues in parasitoid host location

Parasitoid host location in nature is facilitated by simultaneously using different information sources. How multisensory orientation on the same spatial scale is influenced by environmental conditions is however poorly understood. Here we test whether changes in reliability of cues can cause parasitoids to alter multisensory orientation and to switch to cues that are more reliable under extreme temperatures. In the ichneumonid wasp Pimpla turionellae, multisensory use of thermally insensitive vision and thermally sensitive mechanosensory host location by vibrational sounding (echolocation on solid substrate) was investigated with choice experiments on plant-stem models under optimum temperature (18°C), at high- (28°C) and low-temperature limits (8°C) of vibrational sounding. Temperature affected relative importance of vibrational sounding whereas visual orientation did not vary. At 18°C, parasitoids used visual and vibrational cues with comparable relative importance. At 8 and 28°C, the role of vibrational sounding in multisensory orientation was significantly reduced in line with decreased reliability. Wasps nearly exclusively chose visual cues at 8°C. The parasitoids switch between cues and sensory systems depending on temperature. As overall precision of ovipositor insertions was not affected by temperature, the parasitoids fully compensate the loss of one cue provided another reliable cue is available on the same spatial scale.     

Ambient temperature affects mechanosensory host location in a parasitic wasp

Certain parasitic wasps (Ichneumonidae, Pimplinae) use self-produced vibrations transmitted on plant substrate to locate their immobile concealed hosts (i.e. lepidopteran pupae). This mechanosensory mechanism, called the vibrational sounding, depends both on physical cues of the environment and physical activity of the parasitoid and is postulated to depend on ambient temperature. We analysed the influences of temperature on vibrational sounding by choice experiments using plant-stem models with hidden host mimics in the temperate species Pimpla turionellae. The results show a significant effect of temperature on host-location activity and on the success of this process. Outside an optimum range, the performance of the wasps decreased both at low and high temperatures. Below 10°C and beyond 24°C, the wasps displayed (1) substantial reduction in responsiveness, i.e. proportion of females showing ovipositor insertions, (2) reduction of quantitative activity with ovipositor insertions in the individuals, and (3) reduced precision of mechanosensory host location. Nevertheless, female wasps were able to locate their host over a surprisingly broad range of ambient temperatures which indicates that the wasps are able to compensate for temperature effects on vibrational sounding.     

The adaptive significance of host location by vibrational sounding in parasitoid wasps

Vibrational sounding, which is a form of echolocation, is a means of host location by some parasitoid wasps. The wasp taps the substrate (wood, stem or soil) and detects the position of a potential host through the returning 'echoes'. The deployment of vibrational sounding is inferred through the form of the subgenual organ in the female tibia in combination with the presence of modifications to the female antenna used for tapping the substrate. Vibrational sounding and its associated modifications were found in two families. The use of vibrational sounding by parasitoid wasps was positively correlated with the depth of the host in the substrate relative to the size of the parasitoid. There were also significant correlations between the use of vibrational sounding and parasitism of immobile and concealed hosts and between vibrational sounding and idiobiosis. The data suggested that vibrational sounding evolved under a variety of ecological conditions, being employed in the location of wood-boring, stem-boring, soil-dwelling and cocooned hosts and stem-nesting aculeates, often in situations in which the host does not produce vibrations itself.     

Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host

Abstract. The aim of this study was to characterize the vibrations produced by the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae). Host location using vibrations by one of its parasitoids Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) was postulated by Casas (1989) on the basis of detailed quantitative behavioural observations and has also been suggested by other authors on similar systems. Both host and parasitoid send and may receive vibratory signals; consequently we first attempted to characterize and classify the signals, one of the first steps required in the design of an adequate vibrational biotest. In this respect, our approach differs fundamentally from the familiar setting of host location via semiochemicals and is best framed within the context of vibratory communication. Vibrational signals produced by a moving larva and pupa were measured on several spots on the leaf using a laser vibrometer. The emitted signals were characterized by their temporal patterns of change in amplitude and frequency spectra. The vibrational patterns released by a moving larva were different from those released by a wriggling larva and a wriggling pupa in the time as well as in the frequency domains. Wriggling larvae and wriggling pupae triggered vibrations that were similar in frequency, but differed in their temporal pattern. Frequencies up to 15 kHz could be identified. The amplitudes and frequencies of the signals both decreased significantly from the tip to the base of the leaf. A wriggling pupa and a wriggling larva produced stronger signals than a foraging larva. All calculated parameters (displacement, velocity, acceleration, and duration of the signal components) of the vibrational signals were found to be in a range comparable with others used for well-known arthropod communication systems. The vibrations produced by the host displayed distinct characteristics: they could usually be distinguished easily from background noise; could be perceived anywhere on the leaf; and were specific for a certain host stage and activity. Our findings support the hypothesis that vibration signals represent a reliable source of information to foraging parasitoids and, therefore, explain certain behavioural patterns observed in a population of S. sericeicornis females foraging in the field.     

Interaction of vibrational and visual cues in parasitoid host location

Female parasitoids are guided by multisensory information during host finding. Individual cues are used in an interactive or a hierarchical manner according to the relative importance on the spatial scale of their effect. Unlike most studies that concentrate on single cues, the present paper investigates the interaction of two physical cues. The interaction of mechanosensory and visual cues was studied in the pupal parasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae). This species uses, amongst other senses, vibrational sounding (echolocation in a solid substrate) to find its mainly endophytic hosts. Location and frequency of ovipositor insertions were scored on cylindrical plant stem models with single or combined cues. Single-cue experiments show that parasitoids use both visual and mechanosensory cues and achieve a similar precision of host location with either cue. The combination of vision and vibrational sounding increased the precision of host location by a factor of approximately two to three. We conclude that the two senses interact, resulting in an additive accuracy. Neither the visual nor the mechanosensory cue was favored when offered adjacent to each other on the same stem model. On the investigated spatial scale, both physical cues are used and seem to be equally important for host location in this species.     

Stage-dependent strategies of host invasion in the egg-larval parasitoid Chelonus inanitus

Chelonus inanitus (Braconidae) is a solitary egg-larval parasitoid which lays its eggs into eggs of Spodoptera littoralis (Noctuidae); the parasitoid larva then develops in the haemocoel of the host larva. Host embryonic development lasts approx. 3.5 days while parasitoid embryonic development lasts approx. 16 h. All stages of host eggs can be successfully parasitized, and we show here that either the parasitoid larva or the wasp assures that the larva eventually is located in the host's haemocoel. (1) When freshly laid eggs, up to almost 1-day-old, are parasitized, the parasitoid hatches while still in the yolk and enters the host either after waiting or immediately through the dorsal opening. (2) When 1-2-day-old eggs are parasitized, the host embryo has accomplished final dorsal closure and is covered by an embryonic cuticle when the parasitoid hatches; in this case the parasitoid larva bores with its moving abdominal tip into the host. (3) When 2.5-3.5-day-old eggs are parasitized, the wasp oviposits directly into the haemocoel of the host embryo; from day 2 to 2.5 the embryo is still very small and the wasps, after probing, often restrain from oviposition for a few hours.     

Influence of adult experience on host microhabitat location by the generalist parasitoid,Campoletis sonorensis (Hymenoptera: Ichneumonidae)

The effect of adult experience on microhabitat location behavior of the generalist parasitoid Campoletis sonorensis (Cameron)was examined in a wind tunnel bioassay. Responses were tested to the odors of two host plants (cotton and sesame) of Heliothis virescens (F.) or a nonhost plant (potato), either damaged and infested with host larvae and host products (host/plant complex) or intact, clean and uninfested. Parasitoid females remained naive or were allowed one oviposition experience on either of the plants, 1 min, 2 h, or 24 h prior their introduction into the wind tunnel. In a no-choice test, parasitoids experienced 1 min prior to bioassay completed significantly more flights to sesame and potato host/plant complexes than did naive parasitoids. However, 24 h after experience, only females experienced on potato completed more flights to the host/ plant complex than did naive females. Parasitoids experienced 1 min prior to flight to undamaged plants showed a slight increase in flight response (significant only for potato) but, after 24 h, completed only as many flights as naive parasitoids. In a dual-choice situation, parasitoids did not show a preference for either of the two host plants but did prefer a host to a nonhost plant. This innate plant preference was not changed by a single oviposition experience. The potential significance of these results to the microhabitat location behavior of C. sonorensisin the field is discussed.     

Orientation mechanisms and sensory organs involved in host location in a dipteran parasitoid larva

The robber fly Mallophora ruficauda is one of the principal pests of apiculture in the Pampas region of Argentina. Larvae are solitary ectoparasitoids of third-instar scarab beetle larvae. Females of M. ruficauda do not lay eggs on or near the hosts, but on tall grasses. After hatching, larvae are dispersed by the wind and drop to the ground, where they dig and search for potential hosts. It is known that second-instar larvae of M. ruficauda exhibit active host-searching behaviour towards their preferred hosts, i.e., third-instar larvae of Cyclocephala signaticollis. Although host-location seems to be mediated by chemical cues, the mechanism of orientation and the sensory organs involved in host location remain unknown. We carried out behavioural experiments in the laboratory to address these questions. We also tested whether the orientation behaviour is exclusively based on the use of chemical cues. We found that larvae of M. ruficauda detect the chemicals with chemosensilla on the maxillary palps. Only one maxillary palp suffices for orientation, but their bilateral ablation abolishes orientation. Besides, an hexane extract of the host body was as attractive as a live host. Our results support that M. ruficauda larvae find their hosts underground by means of chemoklinotaxis.     

Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two related parasitoid species

Abstract. Parasitoid host range may proceed from traits affecting host suitability, traits affecting parasitoid foraging behaviour, or both. We tested the hypothesis that encapsulation can be used as a reliable indicator of parasitoid host range in two closely related larval endoparasitoids of Lepidoptera. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and a generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). We determined the effects of host species ( Pieris brassicae (L.), P. napi (L.) and P. rapae ) (Lepidoptera: Pieridae) and host developmental stage (early first, second and third instar) on encapsulation of parasitoid eggs. Host species and parasitoid species, as well as the resulting interaction between these two factors had significant effects on encapsulation of Cotesia eggs. Encapsulation in Pieris hosts was much lower for C. glomerata (<34%, except for second and third instar of P. rapae ) than for C. rubecula (>32%), even when the latter was parasitizing P. rapae. Encapsulation increased with the age of the larvae, although the only significant difference was for C. glomerata. Overall, P. rapae showed a stronger encapsulation reaction than P. brassicae and P. napi. Encapsulation levels of C. glomerata corresponded well to patterns of female host species and host age preference for oviposition and parasitoid larval performance. In contrast, percentages of encapsulation of C. rubecula were not consistent with host preference and host suitability. We argue that encapsulation alone is unlikely to provide a sufficient explanation for C. glomerata and C. rubecula host range.     

Effect of wasp size, physiological state, and prior host experience on host-searching behavior in a parasitoid wasp (Hymenoptera: Ichneumonidae)

Host-searching behavior in insects generally varies among individuals. A number of physiological and environmental factors can be involved in such individual variation. Here, a series of behavioral observations were made to highlight the importance of physiological state (i.e., number of mature eggs a female carries, amount of nutrient reserves, etc.) and learning state (i.e., prior host experience) on host-approaching behavior of parasitoids. Itoplectis naranyae (Hymenoptera: Ichneumonidae), a solitary endoparasitoid wasp attacking lepidopteran pupae and prepupae, was used as a test insect. The results show that female wasps with experience ovipositing on hosts 2 days before the test found hosts more quickly than did naïve wasps. Prior experience of host odor itself did not affect host-finding behavior, however. A single oviposition was enough for wasps to shorten time to find a host; additional experience had no significant effect on the efficiency of searching. The number of mature eggs a female carried had no effect on the time required to find a host regardless of prior host experience. The size of wasps, instead, was a significant factor when wasps had no prior host experience, and larger wasps found hosts more rapidly than did smaller wasps. Searching activity was not affected by how many hosts a female wasp had fed on before testing.     

Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid

We examine the effects of fecundity‐limited attack rates and resistance of hosts to parasitism on the dynamics of two‐host–one‐parasitoid systems. We focus primarily on the situation where one parasitoid species attacks two host species that differ in their suitability for parasitism. While all eggs allocated to suitable hosts develop into adult parasitoids, some of the eggs allocated to marginal host do not develop. Marginal hosts can therefore act as a sink for parasitoid eggs. Three‐species coexistence is favoured by low levels of parasitoid fecundity and by low levels of suitability of the marginal host. Our model also produces an indirect (+, ?) interaction in which the suitable host can benefit from the presence of the marginal host, but the marginal host suffers from the presence of the suitable host. The mechanism driving the indirect (+, ?) interaction is egg limitation of parasitoids incurred by allocating eggs to marginal hosts.     

Stopping rule of host search by the parasitoid,Chrysocharis pentheus (Hymenoptera: Eulophidae), in host patches

We studied the stopping rule obeyed by the female parasitoid, Chrysocharis pentheus, in deciding when to leave the leaflet on which she is searching for larvae of Phytomyza ranunculi. She seemed not to employ some stopping rules that have been suggested; i.e., a fixed-number rule and a fixed-time rule and others. The stopping model formulated for Dapsilarthra rufiventris parasitic on the same host species fitted well to the results. The model assumes that the searching female will deposit a marking pheromone on the leaflet at a rate proportional to the search speed and will leave the leaflet when the amount of the pheromone that has accumulated on the leaflet reaches the threshold, L. In this model, L denotes the amount of search effort spent on the leaflet. A comparison of the observed results with the predictions from the model suggested that L increased markedly at the first encounter with the mine (host), but less at later encounters. C. pentheus appears to employ a mixed strategy of a fixed search-effort and an area-concentrated search. This would confer an adaptive advantage in foraging for P. ranunculi larvae, which are distributed in clumps among leaflets in the field.     

Associative learning of complex odours in parasitoid host location

In this paper we address the question how hymenopteran parasitoids deal with complex odour bouquets, using Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) as a model. We examined the capacity of Microplitis croceipes to respond to individual compounds in flight chamber experiments after conditioning parasitoids with a mixture consisting of 2-octanone, methyl jasmonate and beta-caryophyllene. Parasitoids were given a choice between single compounds from the training mixture and beta-ocimene as an unrewarded alternative. When compared with control individuals lacking experience with the odour mixture, parasitoids trained to the odour blend showed an increased preference for 2-octanone and beta-caryophyllene, but not for methyl jasmonate. However, when trained with methyl jasmonate alone, parasitoids were able to respond to this compound. This demonstrates that parasitoids can learn to respond to individual compounds following experience with an odour mixture. However, for certain compounds of a mixture, learning can be blocked by other mixture components. Further experiments in which parasitoids were conditioned and challenged with two compound mixes confirmed that the olfactory background can affect recognition of individual compounds.     

Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology

Asobara japonica (Braconidae) is an endophagous parasitoid developing in Drosophila larvae. The present study shows that A. japonica was never encapsulated in Drosophila melanogaster, and that it caused an overall inhibition of the host encapsulation reaction since injected foreign bodies were never encapsulated in parasitized hosts. Both the number of circulating hemocytes and the phenoloxidase activity decreased in parasitized larvae, and the hematopoietic organ appeared highly disrupted. We also found that A. japonica venom secretions had atypical effects on hosts compared to other braconid wasps. A. japonica venom secretions induced permanent paralysis followed by death of D. melanogaster larvae, whether injected by the female wasp during an interrupted oviposition, or manually injected into unparasitized larvae. More remarkably, these effects could be reversed by injection of ovarian extracts from female wasps. This is the first report that the venom of an endophagous braconid parasitoid can have a deadly effect on hosts, and moreover, that ovarian extracts can act as an antidote to reverse the effects of the wasp's venom. These results also demonstrate that A. japonica secretions from both venom gland and ovary are required to regulate synergistically the host physiology for the success of the parasitoid.     

Importance of sterols acquired through host feeding in synovigenic parasitoid oogenesis

Eupelmus vuilleti (Hymenoptera; Eupelmidae) is a host feeding ectoparasitoid of fourth-instar larvae or pupae of Callosobruchus maculatus (Coleoptera; Bruchidae) infecting Vigna unguiculata seed and pods (Fabacae). Parasitoid females are synovigenic, i.e. they are born with immature eggs and need to feed from the host in order to sustain egg production. In this study, the role of sterols obtained through host feeding in parasitoid oogenesis are examined. Quantitative and qualitative analyses of the sterol contents in each partner of the tritrophic interaction show that a parasitoid female's larval sterol contents is sufficient to produce only 30% of the total number of eggs laid throughout a female's life cycle. In a second step, by manipulating the composition of the sterols hemolymph in the host, it is shown that cholesterol obtained through adult nutrition plays a crucial role in the eggs viability but does not affect the egg production quantitatively. This result has important implications for understanding both the nutrient allocation strategy in this species and the impact of cholesterol in parasitoid reproduction.     

The impact of climatic factors and host density on the long-term population dynamics of vole helminths

Summary The seasonal and long-term population dynamics of helminths parasitizing voles suggested that density-dependent factors might be important in the population dynamics of common species, whereas density-independent factors predominate in the regulation of the rare species. To test this, we used single and multiple regression to analyse the effects of climatic factors and host density on populations of six species of vole helminths over 12 years. The data do support the idea of a difference between common and rare species of helminths, but they clearly do not support the above hypothesis. The common helminths Heligmosomum mixtum (Nematoda) and Catenotaenia sp. (Cestoda) responded to changes in temperature sum (>5° C days) and precipitation during summer. The combined effect of climatic factors and host density explained most of the variation in the long-term dynamics of these common species. By contrast, the long-term dynamics of the rare helminths Paranoplocephala kalelai (Cestoda), Mastophorus muris, Capillaria sp. and Syphacia petrusewiczi (Nematoda) were explained less well by weather and host density than those of the common ones. Furthermore, the common and rare helminths differed in some ways in their responses to climatic factors.     

Multifaceted determinants of host specificity in an aphid parasitoid

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.     

Effect of host size on male fitness in the parasitoid wasp Dinarmus basalis

The effect of host size on male fitness was tested in the parasitoid wasp Dinarmus basalis (Hymenoptera, Pteromalidae) using hosts of different fresh weight. Fitness was measured as the sperm stock in seminal vesicles, and the ability to access females in single or competition situations. Both body size and sperm in seminal vesicles increased with host fresh weight. Males from small hosts had a reduced size and sperm stock compared to those from larger hosts. In single situations, males from both small and large hosts had similar reproductive capacities, whereas in multiple mating or competition situations, males from small hosts were at a disadvantage, inseminating fewer females and copulating less frequently. However, females did not appear to choose between males, and no effect on sperm stored in the spermatheca was observed. Being small does not prevent a D. basalis male mating and producing progeny in single situations, although more offspring could be expected from larger males because of their better competitive abilities.     

Response of insect parasitism to elevation depends on host and parasitoid life-history strategies

How global warming will affect insect parasitoids and their role as natural enemies of insect pests is difficult to assess within a short period of time. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.     

Effect of host density on offspring sex ratios and behavioral interactions between females in the parasitoid waspNasonia vitripennis (Hymenoptera: Pteromalidae)

Pairs of females of the parasitoid waspNasonia vitripennis were videotaped with one or two hosts. The presence of an additional host decreased the number of interactions between females but had no measured effect on the nature of the interactions, i.e., on whether the interaction involved physical contact or occurred while one of the females was parasitizing a host. The number of hosts did not itself affect offspring sex ratios but did influence which other factors were correlated with sex ratio. When there was one host, the proportion of sons was more positively correlated with utilization of previously drilled holes than with female-female interactions, whereas when there were two hosts, the reverse was true. Parasitizing an already parasitized host appeared to affect a female's sex ratio beyond any effects of the physical presence of another female: When two hosts were present, the proportion of sons was greater from hosts parasitized by both females than from hosts parasitized by only one female. The observation that parasitizations in previously drilled holes and female-female interactions are correlated with sex ratios is consistent with previous studies; however, that these relationships are host density dependent is a new result and remains unexplained.