Influence of intrapatch experiences and temperature on the time allocation of the whitefly parasitoidEncarsia formosa (Hymenoptera: Aphelinidae)

The effect of experiences, such as contact with honeydew, rejections of hosts, and ovipositions in hosts, and of temperature on the time allocation of individualEncarsia formosa female parasitoids on tomato leaflets have been studied. Behavioral records were analyzed by means of the proportional hazards model. Analyses were carried out at two levels: (1) the tendency of leaving and (2) the tendency of changing from one leaf side to another. The patch-leaving behavior ofE. formosa can be described by a stochastic threshold mechanism, which is characterized by a certain tendency (probability per time) to leave. The median time from being placed on the leaflet or, if it occurred, from the latest encounter with a host until leaving was 18.6 min. The median time for changing from one leaf side to the other was initially 11.6 min and dropped to 5.7 min after both leaf sides had been visited. The effect of temperature, ranging from 20 to 30°C, was negligible. The presence of honeydew as well as the first oviposition in an unparasitized host decreased the tendency to leave, thus increasing the giving up time (GUT) since the latest encounter with a host. Encounters with parasitized hosts did not affect the GUT since latest encounter; as a result, the total residence time increased. After the first oviposition in an unparasitized host the tendency of changing from the lower leaf side on which hosts were present to the upper side was decreased. The presence of honeydew did not affect the tendency of changing leaf sides.     

Foraging for patchily-distributed leaf miners by the parasitic wasp,Dacnusa sibirica

We studied the rules used by the female parasitoid, Dacnusa sibirica Telenga (Hymenoptera: Braconidae), for deciding when to leave a tomato leaflet on which she is searching for larvae of the leafminer, Liriomyza bryoniae Kalt. (Diptera: Agromyzidae). Females would deposit a marking pheromone on the leaflet and would leave the leaflet when the amount of the pheromone accumulated to the threshold L, which is proportional to the amount of search effort on the leaflet. L appears to increase with host density since it rises after every encounter with a host (or mine).D. sibirica would employ an area-concentrated search, which is advantageous in foraging for hosts showing a clumped distribution.     

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.     

Patch departure mechanisms and optimal host exploitation in an insect parasitoid

1. Patch-leaving decisions are of utmost importance in determining parasitoid foraging success. Parasitoids are known to use both marks left by hosts (chemical or otherwise) and ovipositions to assess host availability and to decide when to leave a host patch.
2. Previous studies have shown that, depending on the species, ovipositions either increase (an incremental mechanism) or decrease (a decremental mechanism) the patch residence times of parasitoids. Reports in the literature conflict on which mechanism is used by Venturia canescens , a parasitoid of pyralid moth larvae.
3. We hypothesize that, as a consequence of saturation in the capacity of the parasitoid to discriminate between host densities at high host numbers, V. canescens uses a decremental mechanism at low host numbers and an incremental one at high host numbers. We call this a 'switching mechanism'.
4. Our experiments show that even if discrimination capacity saturates, V. canescens uses a decremental mechanism over a wide range of host densities.
5. The distribution of hosts in different fruits species under field conditions suggests a switching mechanism would not evolve in natural situations.
6. A model of patch departure in V. canescens is constructed and tested using an independent set of experiments. The model suggests that the patch leaving mechanism in V. canescens is a stochastic decremental one. As might be expected from Weber's Law, the initial leaving tendency is a convex decreasing function of kairomone concentration. The leaving tendency increases exponentially with the time spent in the patch without ovipositing. Ovipositions cause a sudden increase in leaving tendency.
7. Simulations suggest that a decremental mechanism would be out-competed by either one indifferent to ovipositions or an incremental one, only when travel times are much larger than those that are likely to occur in the field.     

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.     

Foraging for patchily-distributed leaf-miners by the parasitoid,Dapsilarthra rufiventris (Hymenoptera: Braconidae). II. Stopping rule for host search

We studied the stopping rule which the female parasitoid,Dapsilarthra rufiventris, uses for deciding when to leave the leaflet on which she is searching for leaf-mining larvae,Phytomyza ranunculi. She is unlikely to employ some current stopping rules, such as fixed-number and fixed-time rules and others. The searching female appears to deposit a marking pheromone on the leaflet. We formulated a model for predicting the amount of pheromone accumulated on the leaflet. The model assumes that she will deposit the pheromone on the leaflet at a given rate (a) per unit time which is proportional to search speed, and will leave it when the amount of pheromone reaches the thresholdL. In this modelL denotes the amount of the search effort spent on the leaflet. The model was fitted fairly well to the data. A comparison of the observed results with the predictions of the model suggests thatL increases markedly at the first encounter with the mine and at a lower rate for the subsequent encounters. This appears to be a kind of area-concentrated search, that is, searching for hosts for a while in the immediate vicinity after finding one host, and would be adaptive in foraging forP. ranunculi larvae, which exhibit clumped distributions among leaflets in the field.     

Analysis of Foraging Behaviour of the Whitefly Parasitoid Encarsia formosa on a plant: A Simulation Study

The foraging behaviour of Encarsia formosa was analyzed using a stochastic simulation model of the parasitoid's behaviour. Parasitoids were allowed to search during a day on a tomato plant infested with immatures of the greenhouse whitefly, Trialeurodes vaporariorum. The model simulates searching, host selection, host handling and patch leaving behaviour, and the physiological state of the parasitoid. The outputs of the model are the number of visited leaflets and the number of hosts encountered, parasitized or killed by host feeding. The simulation results agreed well with observations of parasitoids foraging on tomato plants. The number of encounters and ovipositions on the plant increased with host density according to a type II functional response. At a clustered host distribution over leaflets and low host densities, the most important parameters affecting the number of ovipositions were the leaf area, the parasitoid's walking speed and walking activity, the probability of oviposition after encountering a host, the initial egg load and the ratio of search times on both leaf sides. At high densities, the maximum egg load and the giving-up time on a leaflet since latest host encounter were the most essential parameters.     

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.     

Patch Time Allocation by the Parasitoid <Emphasis Type="Italic">Diadegma semiclausum</Emphasis> (Hymenoptera: Ichneumonidae). II. Effects of Host Density and Distribution

This study investigated the effects of host density and distribution on the patch-leaving behavior of Diadegma semiclausum (Hymenoptera: Ichneumonidae), a solitary endoparasitoid of larval Plutella xylostella (Lepidoptera: Plutellidae). Individual female wasps were released onto an experimental plant infested with host larvae at different densities and distributions, and were allowed to freely leave for an alternative host plant placed upwind of the experimental plant in a wind tunnel. The influence of host density and distribution, as well as within-patch foraging experience, on the parasitoids patch-leaving tendency was analyzed by means of the proportional hazards model. This study aimed to test the predictions of a number of patch-leaving models, including the Marginal Value Theorem, rules of thumb, and incremental or countdown mechanisms. The parasitoids patch-leaving tendency decreased with increased host density, more clustered host distribution, and unsuccessful host encounter as a result of host defense, but increased with successful oviposition. None of the simple rules of thumb such as fixed time, fixed number of hosts parasitized, or fixed giving-up time was employed by this parasitoid. The results agreed with the general predictions of the Marginal Value Theorem that patch residence time and numbers of ovipositions by the parasitoid increased with increasing host density. The decreasing influence of oviposition on the parasitoids patch-leaving tendency, regardless of host density or distribution, was consistent with the prediction of a countdown mechanism.     

Foraging Behaviour and Patch Exploitation by Campoplex dubitator (Hymenoptera: Ichneumonidae), a Parasitoid of Bark-mining Larvae

This study examines the foraging behaviour of Campoplex dubitator Horstmann (Hymenoptera: Ichneumonidae), a parasitoid of the highly concealed bark-mining host, Enarmonia formosana Scopoli (Lepidoptera: Tortricidae), and how this foraging behaviour is affected by host density. The ultimate aim was to determine whether foraging behaviour and patch fidelity could explain patterns of parasitism in the field. An ethogram was first constructed to portray C. dubitator behaviour prior to and immediately following host attacks. The pre-attack behavioural sequence was highly structured whereas behavioural transitions became less predictable after a sting event. Females spent more time on patches with higher host densities and host encounters caused a significant reduction in the leaving tendency. The giving up time was only slightly affected by host encounters. Campoplex dubitator did not demonstrate the ability to distinguish between occupied and empty host mines. The results show that C. dubitator forages more efficiently at lower host densities and this behavioural phenomenon may result in the patterns of parasitism observed in the field.     

Effects of Competition on Optimal Patch Leaving: A War of Attrition

When resources are patchily distributed, animals have to decide when to leave a patch to find a new one. We model this leaving decision for any number n≥2 of animals per patch as a new version of the war of attrition. First, we consider a particular patch and assume that the animals get a fixed gain rate after leaving this patch. In this case, the optimal leaving strategy depends on whether or not there is interference. Without interference, ah animals should leave simultaneously according to the marginal value theorem. With interference, only n−K animals leave simultaneously, where K is a certain number independent of n, and the evolutionarily stable strategy (ESS) of the remaining K animals is stochastic. As a consequence, they may leave at different times, and stay longer than is expected from the marginal value theorem. As the degree of interference increases more animals leave simultaneously, and the leaving tendency of the remaining ones increases as well. The only effect of increasing n is that more animals leave simultaneously. Finally, we discuss in a heuristic way how to use these results in case the gain rate that the animals get after leaving the patch is not fixed but depends on the leaving strategy that is used. When there is no interference, the generalization is straightforward. When there is interference, however, complications arise in deriving the ESS, since the presence of mutants may change the average gain rate in the habitat in such a way that mutants have an advantage over residents. This type of complication also occurs in other ESS derivations where local effects have a strong influence.     

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.     

Comparison of Foraging Behavior, Interspecific Host Discrimination, and Competition of Encarsia formosa and Amitus fuscipennis

The foraging behavior of Amitus fuscipennis MacGown & Nebeker and Encarsia formosa Gahan was studied on tomato leaflets with 20 Trialeurodes vaporariorum (Westwood) larvae in the first or third stage. Ten of the whitefly larvae were previously parasitized and contained a conspecific or a heterospecific parasitoid egg or larva. The host type (host stage and/or previous parasitization) did not influence the foraging behavior of either parasitoid species. The residence time on these tomato leaflets was about 0.9 h for A. fuscipennis and 1.9 h for E. formosa. Amitus fuscipennis hardly stood still and fed little, while E. formosa showed extensive standing still and feeding. As a result, the time walking while drumming was similar for both parasitoid species. The numbers of host encounters and ovipositions per leaflet were similar for both parasitoid species. However, the residence time of A. fuscipennis was half as long as that of E. formosa so the rate of encounters and ovipositions was higher for A. fuscipennis. Amitus fuscipennis is more efficient in finding and parasitizing hosts under these conditions. The walking activity and host acceptance of the synovigenic E. formosa diminished with the number of ovipositions, but not those of the proovigenic A. fuscipennis. Encarsia formosa is egg limited, while A. fuscipennis is time limited because of its short life span and high egg load. Both parasitoid species discriminated well between unparasitized larvae and self-parasitized larvae, but discriminated poorly those larvae parasitized by a conspecific and did not discriminate larvae parasitized by a heterospecific. Self-superparasitism, conspecific superparasitism, and multiparasitism were observed for both parasitoid species. Superparasitism always resulted in the emergence of one parasitoid and multiparasitism resulted in a higher emergence of one parasitoid of the species that had parasitized first. The data suggest that A. fuscipennis is a good candidate for use in biological control of high-density spots of T. vaporariorum when we consider its high encounter and oviposition rate.     

Periodicity,persistence, and collapse in host–parasitoid systems with egg limitation

There is an emerging consensus that parasitoids are limited by the number of eggs which they can lay as well as the amount of time they can search for their hosts. Since egg limitation tends to destabilize host–parasitoid dynamics, successful control of insect pests by parasitoids requires additional stabilizing mechanisms such as heterogeneity in the distribution of parasitoid attacks and host density-dependence. To better understand how egg limitation, search limitation, heterogeneity in parasitoid attacks, and host density-dependence influence host–parasitoid dynamics, discrete time models accounting for these factors are analyzed. When parasitoids are purely egg-limited, a complete anaylsis of the host–parasitoid dynamics are possible. The analysis implies that the parasitoid can invade the host system only if the parasitoid’s intrinsic fitness exceeds the host’s intrinsic fitness. When the parasitoid can invade, there is a critical threshold, CV ^*>1, of the coefficient of variation (CV) of the distribution of parasitoid attacks that determines that outcome of the invasion. If parasitoid attacks sufficiently aggregated (i.e., CV>CV ^*), then the host and parasitoid coexist. Typically (in a topological sense), this coexistence is shown to occur about a periodic attractor or a stable equilibrium. If the parasitoid attacks are sufficiently random (i.e. CV<CV ^*), then the parasitoid drives the host to extinction. When parasitoids are weakly search-limited as well as egg-limited, coexistence about a global attractor occurs even if CV<CV ^*. However, numerical simulations suggest that the nature of this attractor depends critically on whether CV<1 or CV>1. When CV<1, the parasitoid exhibits highly oscillatory dynamics. Alternatively, when parasitoid attacks are sufficiently aggregated but not overly aggregated (i.e. CV>1 but close to 1), the host and parasitoid coexist about a stable equilibrium with low host densities. The implications of these results for classical biological control are discussed.     

Genetic variation in patch time allocation in a parasitic wasp

1. The intra-patch experience acquired by foraging parasitoid females has often been considered to have a strong influence on their tendency to leave a patch, and thus on their total patch residence time. Most studies that have been performed on this subject suggest that the patch-leaving rules observed are adaptive because they enable the females to adjust their patch residence time to local environmental conditions.
2. Considering a behavioural rule as being adaptive supposes that it has been progressively settled by natural selection, and thus that there is, in the population, genetic variation on which the natural selection could act.
3. Therefore, this study aimed to discover whether there was indeed genetic variability in the patch-leaving decision rules in a population of the egg parasitoid species Telenomus busseolae , which attacks patches of its hosts, the eggs of Sesamia nonagrioides . Different wasp families were compared using the isofemale lines method, and the behavioural records were analysed by means of a modified version of the Cox's proportional hazards model proposed by Haccou et al . (1991 ) and Hemerik, Driessen & Haccou (1993 ).
4. The results obtained show that T. busseolae females increase their tendency to leave the patch after each successful oviposition. Each host rejection also led to an increase in the tendency to leave the patch, but this effect was smaller when host rejections were observed between two ovipositions occurring in rapid succession. Subsequent visits to the patch also increased the patch-leaving tendency.
5. Genetic variability was found in both the global patch-leaving tendency and in the effect that successful ovipositions and host rejections have on this tendency.
6. The adaptive and evolutionary consequences of these results are discussed.     

Competitive interaction between two ichneumonid parasitoids of Spodoptera litura

The outcome of competition between Campoletis chlorideae Uchida and Eriborus argenteopilosus (Cameron) (Hymenoptera: Ichneumonidae), two indigenous larval parasitoids of the noctuid pest, Spodoptera litura (Fabricius), was investigated in the laboratory by way of two experiments. In the individual exposure experiment, the host larvae were exposed to the parasitoids either alone or one after the other at different time intervals and were considered to be parasitised when the parasitoid was observed to sting the host larva. When they stung the host larva singly, the parasitism rates by C. chlorideae and E. argenteopilosus was either similar to or higher than the parasitism recorded by each parasitoid in the different combination/interaction treatments. C. chlorideae cocoons were formed from majority of the host larvae, which were stung by both parasitoid species, one after the other, in most oviposition orders and delays between ovipositions. E. argenteopilosus appeared to be the dominant parasitoid only in those treatments where it was the first one to parasitise and the delay in C. chlorideae parasitism was more than 18 h. and it never dominated the interactions, when it was the second one to parasitise. This implied that C. chlorideae had an almost consistent advantage over E. argenteopilosus. In the mass exposure experiment, the two parasitoid species (either alone or together) were allowed to forage and parasitise the host larvae in cages. When the two parasitoid species were allowed to forage in the same host patch simultaneously, the performance of C. chlorideae when it was alone was statistically similar to its performance in the presence of E. argenteopilosus. However, E. argenteopilosus performed better when it could forage alone. The results of both experiments revealed that C. chlorideae was the more competitive of the two species.     

Patch residence decisions made by Aphidius colemani in the presence of a facultative predator

One of the key questions in ecology is how animals optimally allocate their time in an environment with patchily distributed resources and competing organisms. Here we investigate the effects that an aphid predator, Macrolophus caliginosus (Wagner) (Hemiptera: Miridae), has on the searching behavior and the patch residence decisions of an aphid parasitoid, Aphidius colemani (Viereck) (Hymenoptera: Aphidiidae). A computer programme was designed that allowed the recording and saving of direct observations. The time allocated to different activities by a female parasitoid wasp in the presence or absence of the predator M. caliginosus was investigated. The experiments were conducted under controlled environment conditions using leaves of sweet pepper, Capsicum annuum L. (Solanaceae) and Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the host plant–prey species system. The parasitoid spent significantly less time on ‘secondary’ activities, such as preening and resting, when the predator was present. Survival analysis showed that the parasitoid had a higher patch-leaving tendency when the predator was present.     

Early oviposition experience affects patch residence time in a foraging parasitoid

Parasitoids learn olfactory and visual cues that are associated with their hosts, and use these cues to forage more efficiently. Classical conditioning theory predicts that encounters with high-quality hosts will lead to better learning of host-associated cues than encounters with low-quality hosts. We tested this prediction in a two-phase laboratory experiment with the parasitoid Trichogramma thalense Pinto & Oatman (Hymenoptera: Trichogrammatidae) and the host Anagasta kuehniella Zeller (Lepidoptera: Pyralidae).Host quality during the first exposure to hosts affected later foraging behavior for some experimental treatments, as predicted. We used a learning model, followed by patch-time optimization, to interpret our findings. We first simulated the parasitoids' host encounters during the experiment, and predicted their estimate of patch quality after each encounter. We then used dynamic optimization to predict the parasitoids' optimal patch residence times. The model reproduces the trends of the experimental results.     

Larvicidal activity of lectins onLucilia cuprina: mechanism of action

Foraging behaviour and host-instar preference of young and old females of the solitary aphid parasitoid,Lysiphlebus cardui Marshall (Hymenoptera: Aphidiidae), were studied in the laboratory. The analysis of interactions between parasitoids and different stages ofAphis fabae cirsiiacanthoidis Scop. (Homoptera: Aphididae) revealed that encounter rates between aphids and parasitoid females and defence reactions of the aphids influenced the degree to which a particular aphid age class is parasitized. Encounter rates between hosts and parasitoid females depended on the foraging pattern of the parasitoid, which varied with age. In mixed aphid colonies patch residence time increased with parasitoid age. Furthermore, younger parasitoids (≦1 day old) laid more eggs into second and third instars, while older parasitoids (≧4 days old) did not show distinct host instar preferences. It is suggested that the oviposition behaviour ofL. cardui is influenced by the physiological state, i.e. the age of the wasp.     

Superparasitism as a differential game

Superparasitism refers to a female parasitoid laying an egg in a host already parasitized by a conspecific. In solitary species, only one offspring per host is expected to complete development, hence the game. Hosts are often clumped in patches and several females exploiting such an aggregate of resource make its state change over time, hence the dynamical character of the game. Two coupled questions arise: (i) Is it worth accepting a parasitized host? (ii) When to leave the host patch? Through these decisions (i) the competition for healthy hosts and (ii) the trade-off between leaving in quest of a better patch and staying to make the patch less profitable for other parasitoids (this is a way to lower superparasitism likely to occur after having left the patch) are addressed. The aim of this work is to characterize a strategy that would be evolutionarily relevant in such a situation, as it directly concerns females' reproductive success. Investigating a (synchronous) nonzero-sum two-player differential game allows us to characterize candidate dynamic evolutionarily stable policies in terms of both oviposition and patch-leaving decisions. For that matter, the game is (in the most part of the parameter space) completely solved if the probability that superparasitism succeeds is assumed to be close to one-half, a fair value under direct competition. The strategic equilibrium consists, for each females, in (i) superparasitizing consistently upon arrival on the patch, and (ii) leaving when the loss of fitness due to superparasitism likely to occur after its departure is reduced to zero. The competing females are thus expected to leave the patch as they arrived: synchronously. Superparasitism does not necessarily lead to a war of attrition.