Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). III. Effects of Kairomone Sources and Previous Parasitism

We investigated the effects of kairomone sources and previous parasitism on the patch-leaving behavior of Diadegma semiclausum, a solitary endoparasitoid of larval Plutella xylostella. Individual female wasps were released onto an experimental plant, and were allowed to freely leave for an alternative host plant placed upwind of the experimental plant in a wind tunnel. In one experiment, the experimental plant was either intact, contained host damage alone, or contained both hosts and host damage. In another experiment, the plant was infested with either unparasitized hosts, hosts parasitized previously by the female herself, or parasitized by Cotesia plutellae, another larval endoparasitoid of P. xylostella. We analyzed the influence of kairomone sources, host types, and within-patch foraging experience on the patch-leaving tendency of D. semiclausum by means of the proportional hazards model. Presence of host damage, and unsuccessful host encounters as a result of host defenses decreased the parasitoids' patch-leaving tendency, while successful oviposition, self-superparasitism, and rejection of parasitized hosts increased their patch-leaving tendency. A conceptual model of the parasitoid's patch-leaving behavior is proposed on the basis of the results of current and previous studies.     

Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs

Learning, defined as changes in behavior that occur due to past experience, has been well documented for nearly 20 species of hymenopterous parasitoids. Few studies, however, have explored the influence of learning on population-level patterns of host use by parasitoids in field populations. Our study explores learning in the parasitoid Aphidius ervi Haliday that attacks pea aphids, Acyrthosiphon pisum (Harris). We used a sequence of laboratory experiments to investigate whether there is a learned component in the selection of red or green aphid color morphs. We then used the results of these experiments to parameterize a model that examines whether learned behaviors can explain the changes in the rates of parasitism observed in field populations in South-central Wisconsin, USA. In the first of two experiments, we measured the sequence of host choice by A. ervi on pea aphid color morphs and analyzed this sequence for patterns in biased host selection. Parasitoids exhibited an inherent preference for green aphid morphs, but this preference was malleable; initial encounters with red aphids led to a greater chance of subsequent orientation towards red aphids than predicted by chance. In a second experiment, we found no evidence that parasitoids specialize on red or green morphs; for the same parasitoids tested in trials separated by 2 h, color preference in the first trial did not predict color preference in the second, as would be expected if they differed in fixed preferences or exhibited long-term (> 2 h) learning. Using data from the two experiments, we parameterized a population dynamics model and found that learning of the magnitude observed in our experiments leads to biased parasitism towards the most common color morph. This bias is sufficient to explain changes in the ratio of aphid color morphs observed in field sites over multiple years. Our study suggests that for even relatively simple organisms, learned behaviors may be important for explaining the population dynamics of their hosts.     

Foraging Behavior and Patch Time Allocation by Fopius arisanus (Hymenoptera: Braconidae), an Egg-Larval Parasitoid of Tephritid Fruit Flies

This study quantitatively describes the host-searching behavior of Fopius arisanus (Sonan) (Hymenoptera: Braconidae), an important egg-larval parasitoid of tephritid fruit fly pests, on coffee berries infested with host eggs of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). We also investigate the parasitoid's response to local variation in host patch quality. The temporal pattern of behavioral organisation was examined by constructing an ethogram. The parasitoid spent over 90% of its foraging time in detecting and locating hosts after arriving on a host-infested fruit, and displayed a relatively fixed behavioral pattern leading to oviposition. Patch residence time increased in the presence of host-associated cues, following successful ovipositions, and with increasing size of host clutches per fruit, but decreased with each successive visit to the same host patch and with increasing availability of alternative host patches. The parasitoid females discriminated against previously parasitized hosts and spent significantly less time and searching effort on patches previously exploited by herself or by conspecific females. The effective host-searching behavior, perfect host discrimination ability, and success-motivated searching strategy shown by F. arisanus ensured a thorough exploitation of host resources by this parasitoid.     

Parasitoids use herbivore-induced information to adapt patch exploitation behaviour

Abstract.  1. Optimal foraging models ultimately predict that female parasitoids should exploit rich host patches for longer than poorer ones. At the proximate level, mechanistic models and experimental studies show that parasitoids use both chemicals produced by their hosts and direct encounters with their hosts to estimate patch quality. Although it has been extensively studied in the context of host location, the use of herbivore-induced plant response by insect parasitoids has never been considered in the context of patch time allocation.
2. In this study, the respective roles of herbivore-induced plant response and direct contact with hosts on the foraging behaviour of Lysiphlebus testaceipes females on an aphid patch were quantified. For this, the level of herbivore-induced plant response and the number of aphids on the leaf bearing the patch were manipulated independently. Different levels of plant response were obtained by varying the duration of infestation on another leaf.
3. Parasitoid residence time and number of attacks increased with both the level of plant response and the number of aphids.
4. These results suggest that L. testaceipes females use the combination of herbivore-induced response of plants and direct encounters with hosts to assess patch quality and adjust their patch use behaviour.     

Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus

Abstract.

• 1 The ability to use flexible decision rules can be an advantage to parasitoid females searching for patchily-distributed hosts. In a series of laboratory experiments the hypothesis that Opius dimidiatus, a solitary parasitoid of the chrysanthemum leafminer (Liriomyza trifolii), adjusts the time she allocates to searching for her larval hosts in response to both patch qualities and experiences with hosts was tested by varying such patch parameters as area, presence of host mines and density of host mines, and by allowing ovipositions and encounters with parasitized hosts.
• 2 Though leaf area was not a factor, the presence of host mines in a leaf did increase the time a female O.dimidiatus spent searching, over time spent on unmined leaves.
• 3 When host mine density was increased, females responded by increasing their search period in a density-dependent manner, suggesting a perception of patch quality.
• 4 Ovipositions in hosts caused females to reset their‘giving-up time’(GUT), or increase search intensity, by adding an amount of search time that increased with each successive oviposition. Conversely, encounters with parasitized (unsuitable) hosts incremented the GUT, but by an amount that decreased with each successive encounter.

     

Visual and Chemical Cues Used in Host Location and Acceptance by a Dipteran Parasitoid

Locating potential hosts for egg laying is a critical challenge in the life history of many insects. Female insects in several orders have evolved mechanisms to find hosts by using olfactory and visual signals derived from their hosts. We describe visual and chemical cues used by the dipteran parasitoid Apocephalus paraponerae (Diptera: Phoridae) in the location and acceptance of its host ant Paraponera clavata (Hymenoptera: Formicidae: Ponerinae). Our results show that A. paraponerae uses the visual cue of ant body size when locating hosts at short range and that these flies lay more eggs in ants that retain their surface chemicals than in ants with these chemicals removed. We compare the cues used by A. paraponerae with cues used by tephritid fruit flies in location and acceptance of their hosts, and we suggest further avenues for the study of host location, acceptance, and host discrimination of A. paraponerae and other parasitoids of ants.     

Learning in the Generalist Tachinid Parasitoid Exorista Mella Walker (Diptera: Tachinidae)

Many parasitoids have been shown to learn visual and/or olfactory cues associated with hosts. In contrast to the Hymenoptera, learning in dipteran parasitoids is relatively unstudied. This study explores the ability of a polyphagous tachinid, Exorista mella, to learn to associate visual and olfactory cues with hosts. In an experiment involving colored host models, flies trained on models of one color were subsequently attracted more strongly to models of the color that they had not experienced. The unsuitability of these models as hosts suggested that the flies may have engaged in avoidance learning. Flies demonstrated the ability to learn to associate colored disks with hosts. A separate experiment demonstrated that flies responded to volatile plant compounds but failed to find evidence for odor learning. Learning of host-associated cues by E. mella may allow this generalist parasitoid to take advantage of locally abundant host populations and maintain host-searching efficiency in an environment.     

Patch time allocation in male parasitoids

Abstract 1. Patch time allocation has been mostly studied in female parasitoids exploiting patches of hosts. Different parameters such as oviposition, host encounters, patch quality, etc. have been repeatedly shown to modify the time females invest on hosts. 2. Male parasitoids are expected to maximise their lifetime fitness by maximising the number of females inseminated during their life. Because they can be sperm and/or time limited, they should optimise their time allocation on emergence patches. 3. Patch time allocation thus appears to be an important question for both male and female parasitoids. 4. In this study, we determined the parameters used by males of the egg parasitoid Trichogramma turkestanica to decide when to leave the emergence patch. Among the different patch‐leaving parameters tested, only contacts with parasitised hosts and presence of virgin females significantly influenced the patch‐leaving tendency. 5. Our results suggest that males express behaviours that could enable them to optimise their patch exploitation time, as females do, but using different strategies.     

Interspecific interference between Apoanagyrus lopezi and A. diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti

The parasitoids Apoanagyrus lopezi De Santis and A. diversicornis (Howard) (Hymenoptera: Encyrtidae) have been introduced into Africa for the biological control of the cassava mealybug Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae). We have studied competition between these species to investigate if they can coexist. Here we report on the influence of the simultaneous presence of non-conspecific adult females on searching efficiency on patches. Wasps of either species foraged on discs of cassava leaf with mealybugs, while at the same time different numbers of non-conspecifics were also depleting the patch. Patch area per parasitoid and number of hosts available to each parasitoid were equal in all treatments.In both species, the presence of other foragers clearly affected several aspects of the parasitoids' behaviour. Patch residence time increased with the number of non-conspecifics in A. diversicornis. In both parasitoid species, the proportion of hosts left unparasitized after the patch visit decreased with increasing numbers of females on the patch. The proportions of super- and multiparasitism did not change with the number of females. Both species produced more offspring during a patch visit in the presence of more non-conspecifics. These behavioural changes did not, however, lead to a change in the offspring production rate on patches. A. diversicornis produced offspring at a rate three times that of A. lopezi when one A. lopezi and one A. diversicornis foraged simultaneously. This is the first report of an aspect of interspecific competition where A. diversicornis has an advantage over A. lopezi. Interference between adult females thus promotes coexistence of the two species on P. manihoti.     

Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors

Parasitoids exploit numerous chemical cues to locate hosts and food. Whether they detect and learn chemicals foreign to their natural history has not been explored. We show that the parasitoid Microplitis croceipes can associate, with food or hosts, widely different chemicals outside their natural foraging encounters. When learned chemicals are subsequently detected, this parasitoid manifests distinct behaviors characteristic with expectations of food or host, commensurate with prior training. This flexibility of parasitoids to rapidly link diverse chemicals to resource needs and subsequently report them with recognizable behaviors offers new insights into their foraging adaptability, and provides a model for further dissection of olfactory learning related processes.     

Pre‐Patch Experience Affects the Egg Distribution Pattern in a Polyembryonic Parasitoid of Moth Egg Batches

According to foraging theory, female parasitoids should alter their host choice in response to cues that indicate a limitation of resources. We tested whether females of the polyembryonic parasitoid Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), which attack egg batches of small ermine moths (Lepidoptera: Yponomeutidae), would alter their host acceptance pattern in response to different pre‐patch experience. We kept females of the parasitoid prior to a patch visit under different conditions, which should indicate different levels of competition for hosts. With increased competition as pre‐patch experience, females laid more eggs per host egg and self‐superparasitized more often, and the resultant egg distributions showed a trend from more regular distributions to increasingly Poisson and aggregated distributions. Consequently, females with a pre‐patch experience that would indicate low competition for hosts had the most even egg distributions. We conclude that pre‐patch experience of competitors may lead to a significant change of mutual interference patterns in egg‐laying A. fuscicollis wasps.     

Motivation models fail to explain oviposition behaviour in the diamondback moth

Abstract. It is widely accepted that previous experience and internal physiological factors (such as egg‐load) affect host‐plant discrimination during oviposition by phytophagous insects. However, there is some debate as to how these factors interact in a mechanistic sense to control acceptance. The role of learning and host deprivation in host acceptance by adult diamondback moths (Plutella xylostella L.) was investigated. In the first experiment, we tested whether experience of a lower ranked host cabbage increased acceptance of a higher ranked host as predicted by a hierarchy threshold model. Moths trained on cabbage were over three times more likely to accept cabbage during testing than untrained moths. There was no effect of cabbage training on acceptance of cress, indicating that the effect of training was species‐specific. In a second experiment, designed to test the prediction of motivation models that insects become less discriminating when deprived of oviposition opportunities, depriving females of host plants for 2 nights significantly increased female egg‐load (×2.3). Host deprivation did not decrease discrimination between the preferred host cress and cabbage. Cabbage and cress plants were equally likely to have been accepted by nondeprived moths after 1 night of exposure, yet moths deprived of hosts for 2 nights strongly preferred cress when tested during the first 20 min of the scotophase. During this 20‐min period, previous host deprivation increased acceptance of host plants generally but did not decrease discrimination between hosts. These data contradict the expectation that there is an inverse relationship between host species discrimination and the failure of an insect to find hosts as found in existing oviposition acceptance models. As an alternative, the Incremental Acceptance Model of host acceptance behaviour is presented, in which responsiveness to a host is a function of the recent encounter rate with host‐specific stimuli, and the oviposition reflex is regulated by nonspecific cues such as egg‐load.     

Choosing suitable hosts: common cuckoos Cuculus canorus parasitize great reed warblers Acrocephalus arundinaceus of high quality

We investigated the hypothesis that the common cuckoo Cuculus canorus selects host pairs of good phenotypic quality. As there is some evidence that cuckoos may select hosts within a population non-randomly based on external cues reflecting their foster abilities, we predicted that great reed warbler Acrocephalus arundinaceus pairs parasitized by the cuckoo would exhibit higher quality than unparasitized ones. To test this assumption, we evaluated two different parameters indicating host quality: body condition and characteristics of host eggs. We found that parasitized females showed significantly better body condition than unparasitized ones, and the model showed that the probability of being parasitized by the cuckoos increased with increasing body condition. Moreover, the likelihood of being parasitized by a cuckoo within the great reed warbler population increased with decreasing colour variability within clutches: parasitized females allocated costly blue pigments to eggshells more equally compared with unparasitized ones. Our study revealed that cuckoos parasitize great reed warbler females of higher quality, as reflected in host body condition and egg colour characteristics. In highly mimetic systems, cuckoos may choose to parasitize hosts with eggs displaying low intraclutch variation, both because this leads to reduced rejection and because these hosts are of high quality.     

Patch Time Allocation by the Parasitoid Diadegma semiclausum (Hymenoptera: Ichneumonidae). I. Effect of Interpatch Distance

We observed the foraging behavior of Diadegma semiclausum (Hymenoptera:Ichneumonidae), a larval parasitoid of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae), in a wind tunnel to determine how interpatch distance affects patch time allocation. Individual female wasps were released onto an experimental patch infested with host larvae and were allowed freely to leave for an identically extrapatch placed upwind of the experimental patch with varying interpatch distances. The effects of interpatch distance and within-patch foraging experience on the patch-leaving tendency of the parasitoid were analyzed bymeans of the proportional hazards model. Increasing interpatch distance andunsuccessful host encounter as a result of host defense decreased the patch-leaving tendency, while successful oviposition and unsuccessful search time since last oviposition increased the patch-leaving tendency. Asa result, both patch residence time and number of ovipositions by D. semiclausum increased with increasing interpatch distance, which appears to agree with the general predictions of the marginal value theorem that a parasitoid should stay longer and parasitize more hosts with increasing interpatch distance.     

Two tachinid species discriminate between parasitized and non-parasitized hosts

The abilities ofMyiopharus doryphorae (Riley) andM. aberrans (Townsend) (Diptera: Tachinidae) to discriminate between parasitized and non-parasitized Colorado potato beetle (host)Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) larvae, were investigated under laboratory and field conditions. Laboratory experiments showed that bothMyiopharus species have a significantly greater frequency for larvipositing in non-parasitized hosts over parasitized ones. Direct field observations of larvipositional behavior of bothMyiopharus species over three growing seasons showed effective restraint from larviposition into parasitized hosts, while larviposition into nonparasitized ones occurred readily. Avoidance of previously-parasitized hosts occurred after the larvipositing flies briefly landed on host larvae without attempting to insert the larvipositor. The low levels of superparasitism which occurred in the caged experiments and in the field appeared to be due to a breakdown of the larvipositing parasitoids' restraint when they met only parasitized hosts or when many parasitoids competed for reduced numbers of hosts late in the season.     

Host location and selection cues in a generalist tachinid parasitoid

Tachinid flies are diverse and ecologically important insect parasitoids. However, the means by which tachinid species locate and select hosts are poorly known. Many tachinids exhibit unusually wide host ranges and they also possess well-developed visual systems. These characteristics suggest that tachinids differ from parasitic wasps in their reliance on various sensory modes and types of cues. A series of behavioral assays using the generalist tachinid Exorista mella Walker (Diptera: Tachinidae) were conducted to examine what types of cues this parasitoid uses to locate and accept hosts, and how the cues used may reflect its ecological relationships with hosts. Female E. mella responded strongly to host motion in assays using both live hosts and host corpses, and this cue is shown to be an important elicitor of attack behavior. Females also responded to volatile chemicals associated with damaged food plants of their host in an olfactometer. Flies responded only weakly to direct visual contact with stationary hosts and odors directly associated with hosts. The behavior of female E. mella changed with experience such that more experienced flies recognized and attacked hosts more readily than did inexperienced flies. The use of general olfactory and visual cues by E. mella may be an effective strategy by this polyphagous parasitoid to locate a broad range of potential hosts.     

Analysis of foraging behavior of the whitefly parasitoidEncarsia formosa (Hymenoptera: Aphelinidae) in an experimental arena: A simulation study

Foraging ofEncarsia formosa was analyzed using a stochastic simulation model of the parasitoid's behavior. Parasitoids were allowed to search during a fixed time in an experimental arena with immatures of the greenhouse whitefly,Trialeurodes vaporariorum. The model simulates host searching, selection, and handling behavior and the physiological state (egg load) of the parasitoid. The simulated number of hosts encountered, parasitized, or killed by host feeding agreed well with observations on leaf disks. The hypothesis of random host encounter seems to be correct. The number of ovipositions on the leaf at low host densities was strongly affected by the parasitoid's walking speed and walking activity, the probability of oviposition after encountering a host, and the initial egg load. At high densities, the initial and maximum egg load were most important. A strong temperature effect was found at 18°C or below. The number of encounters, ovipositions, and host feedings increased with host density to a maximum of 25, 6.5, and 1.5, respectively, during 2 h at 25°C. The shape of the curves resembled a Holling Type II, which may be the result of the experimental procedure, where a parasitoid was confined to a patch during a fixed time.     

The role of herbivore‐ and plant‐related experiences in intraspecific host preference of a relatively specialized parasitoid

Parasitoids use odor cues from infested plants and herbivore hosts to locate their hosts. Specialist parasitoids of generalist herbivores are predicted to rely more on herbivorederived cues than plant-derived cues. Microplitis croceipes (Cresson)(Hymenoptera: Braconidae) is a relatively specialized larval endoparasitoid of Heliothis virescens (F.)(Lepidoptera: Noctuidae), which is a generalist herbivore on several crops including cotton and soybean. Using M. croceipes/H. virescens as a model system, we tested the following predictions about specialist parasitoids of generalist herbivores:(i) naive parasitoids will show innate responses to herbivore-emitted kairomones, regardless of host plant identity and (ii) herbivore-related experience will have a greater influence on intraspecific oviposition preference than plant-related experience. Inexperienced (naive) female M. croceipes did not discriminate between cotton-fed and soybean-fed H. virescens in oviposition choice tests, supporting our first prediction. Oviposition experience alone with either host group influenced subsequent oviposition preference while experience with infested plants alone did not elicit preference in M. croceipes, supporting our second prediction. Furthermore, associative learning of oviposition with host-damaged plants facilitated host location. I terestingly, naive parasitoids attacked more soybeathan cotton-fed host larvae in two-choice tests when a background of host-infested cotton odor was supplied, and vice versa. This suggests that plant volatiles may have created an olfactory contrast effect. We discussed ecological significance of the results and concluded that both plant- and herbivore-related experiences play important role in parasitoid host foraging.     

Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism

Abstract.

• 1 The pay-off from an egg laid in a parasitized host is an important parameter in models on adaptive superparasitism in solitary insect parasitoids.
• 2 For Leptopilina heterotoma, a parasitoid of larval Drosophila, the pay-off from a second egg laid in a host is 0.43 offspring when the interval between the two ovipositions is less than 3h. For longer intervals, this pay-off decreases to almost zero for an interval of 24 h.
• 3 When a female encountering a parasitized host is able to estimate the interval since the first oviposition, it is expected that she will take this into account in her host selection decisions. This is, however, not in the direct interest of the female that lays the first egg, and marks the host.
• 4 We studied whether superparasitism in hosts containing a young egg is more common than in hosts containing an older egg, when searching in a patch containing once-parasitized and unparasitized hosts.
• 5 The acceptance/encounter ratio of parasitized hosts increased for intervals longer than 6h, as predicted when the interests of the marking female and the longevity of the mark are taken into account.
• 6 Superparasitism occurred more often when parasitoids had previously searched a host patch 7 days before the experiment compared to when parasitoids had searched a patch 1 day before, a phenomenon predicted by dynamic optimal diet models.

     

Herbivore-induced plant volatiles as cues for habitat assessment by a foraging parasitoid

1. Animals usually require information about the current state of their habitat to optimize their behaviour. For this, they can use a learning process through which their estimate is continually updated according to the cues they perceive. Identifying these cues is a long-standing but still inveterate challenge for ecologists. 2. The use of plant cues by aphid parasitoids for the assessment of habitat profitability and the adaptation of patch exploitation was studied. Grounding on predictions from optimal foraging theory, we tested whether parasitoids exploited host patches less intensively after visiting heavily infested plants than after visiting plants bearing fewer aphids. 3. As predicted, after visiting heavily infested plants parasitoids reduced their residence time and attacked fewer hosts in the next patch. This was the case regardless of whether the aphids were actually present on the first plant, indicating that the cue came from the plant. Moreover, the level of infestation of a plant at some distance from the first plant visited affected parasitoid patch exploitation on the second plant in a similar manner, indicating that the cue was volatile. 4. These results highlight a novel role of herbivore-induced volatiles in parasitoid foraging behaviour, different from the widely studied attraction at a distance.