Olfactory host location and learning in the granary weevil parasitoidLariophagus distinguendus (Hymenoptera: Pteromalidae)

The sources of volatiles that attract the parasitoid Lariophagus distinguendus(Först.) to its hosts, the larvae of the granary weevil Sitophilus granarius(L.) infesting grains of Triticum aestivumL., were investigated in bioassays. The influence of oviposition experience on the responsiveness of the parasitoids to the sources of volatiles was considered. The potential sources of attractants are the host larvae, their feces, and the grain infested by the host. Weevil larvae were not attractive. Feces were attractive to females without and females with oviposition experience. Infested grains from which the larvae and feces were removed were slightly attractive to inexperienced, but very attractive to experienced females. Healthy and artificially damaged grains were attractive to experienced parasitoids only. Refering to the “variable response model,” we discuss the effect of experience on the response of the parasitoids to the several stimuli. Stimuli from different trophic levels are used by the foraging parasitoids: feces of the host larvae is an important source of attractants, but also the grains, particularly after experience.     

Inverse density dependent parasitism in a patchy environment: a laboratory system

Abstract. 1. Two species of parasitoids (Anisopteromalus calandrae (Howard) and Heterospilus prosopidis Vier) attacking the bruchid beetle, Callosobruchus chinensis (L.), show marked inverse density dependent relationships between per cent parasitism and host density per patch.
2. These patterns are well described quantitatively using data on the spatial distribution of searching time by the parasitoids and their attack rates on patches of different host density.
3. A model of optimal foraging predicts just the opposite (i.e. density dependent) patterns of parasitism.
4. Both density dependent and inversely density dependent spatial patterns of parasitism can be explained mechanistically in terms of (a) the allocation of searching time in patches of different host density and (b) the maximum attack rate per parasitoid that constrains the extent of host exploitation within a patch.     

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.     

Identifying bird cherry-oat aphid Rhopalosiphum padi emigrants, alate exules and gynoparae: application of multivariate methods to morphometric and anatomical features

The host microhabitat location behavior of females of the generalist parasitoid Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae) was studied in a wind tunnel. Visual cues associated with the host plant cotton, Gossypium hirsutum L., were important and significantly more parasitoids completed flights to a damaged 4-leaf cotton plant bearing a Heliothis virescens (F.) (Lepidoptera: Noctuidae) larva and frass than to a similarly damaged single leaf with frass and a larva. This difference in completed flights was not due to differences in amounts of volatiles released by the two stimuli. Both naive and experienced parasitoids responded differently to an undamaged cotton leaf, a mechanially damaged leaf, a naturally damaged leaf with the host removed and a naturally damaged leaf with a host larva. Parasitoids completed significantly fewer flights to the undamaged sources of volatiles than to damaged sources of volatiles. Experienced females responded strongly to all types of damage. The number of flights completed by naive females to the three types of damage differed but not significantly and was less than the number completed by experienced females. Components of the preflight experience were varied to determine which factors were responsible for the higher response of experienced females to the host/plant complex. Oviposition was the most important component of this experience. Contact with host frass or plant damage followed by oviposition did not increase the response over that exhibited by females allowed oviposition only. When frass or damaged plant material were contacted without subsequent oviposition, females completed fewer flights than naive females.     

Host relations, life cycles and multiparasitism in some parasitoids of aphidophagous Syrphidae (Diptera)

Abstract. 1. Records of parasitism from the field and host choice experiments suggest that most parasitoids of syrphids are monophagous. A few are oligophagous.
2. To elicit egg release, females require a stimulus from the host haemolymph. Differential response to haemolymph cues by females may account for the observed pattern of host relations.
3. Differences in host ranges and timing of female flight periods probably characterize most of the parasitoids studied.
4. In one case of two monophagous parasitoids, Diplazon pectoratorius (Thunberg) and Syrphophilus tricinctorius (Thunberg) attacking the same host Syrphus ribesii (L.) no partitioning was found. Stricinctorius is, however, a superior intrinsic competitor.     

Age-dependent clutch size in a koinobiont parasitoid

Abstract.  1. The Lack clutch size theory predicts how many eggs a female should lay to maximise her fitness gain per clutch. However, for parasitoids that lay multiple clutches it can overestimate optimal clutch size because it does not take into account the future reproductive success of the parasitoid.
2. From egg-limitation and time-limitation models, it is theoretically expected that (i) clutch size decreases with age if host encounter rate is constant, and (ii) clutch size should increase with host deprivation and hence with age in host-deprived individuals.
3. Clutch sizes produced by ageing females of the koinobiont gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) that were provided daily with hosts, and of females ageing with different periods of host deprivation were measured.
4. Contrary to expectations, during the first 2 weeks, clutch size did not change with the age of the female parasitoid, neither with nor without increasing host-deprivation time.
5. After the age of 2 weeks, clutch size decreased for parasitoids that parasitised hosts daily. The decrease was accompanied by a strong decrease in available eggs. However, a similar decrease occurred in host-deprived parasitoids that did not experience egg depletion, suggesting that egg limitation was not the only factor causing the decrease in clutch size.
6. For koinobiont parasitoids like M. tristis that have low natural host encounter rates and short oviposition times, the costs of reproduction due to egg limitation, time limitation, or other factors are relatively small, if the natural lifespan is relatively short.
7. Koinobiont parasitoid species that in natural situations experience little variation in host density and host quality might not have strongly evolved the ability to adjust clutch size.     

Patterns of parasitism by insect parasitoids in patchy environments

Abstract. 1. This paper shows how the different spatial patterns of per cent parasitism in patches of different host density can be explained within a single model framework that takes into account the parasitoid's aggregative response, and the factors limiting the degree of host exploitation within patches.
2. Two contrasting laboratory examples are presented in which the distribution of searching parasitoids and the resulting levels of parasitism in different patches are both known for a range of parasitoid densities.
3. A model is described predicting the number of hosts parasitized per patch, in which the number of parasitoids searching is determined from a simple expression allowing different degrees of aggregation.
4. The model generates patterns of parasitism encompassing the two laboratory examples and a wide range of examples from the field.
5. The importance of density dependent spatial distributions of parasitism to population stability is briefly discussed.     

Searching and oviposition behaviour of Amitus fuscipennis, a parasitoid of the greenhouse whitefly

Abstract: Amitus fuscipennis MacGown & Nebeker (Hym., Platygasteridae) is a parasitoid of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Hom., Aleyrodidae) on some crops as bean and snap bean (both Phaseolus vulgaris L.) in Colombia. The searching and oviposition behaviour of A. fuscipennis was studied in the laboratory, using T. vaporariorum as a host on bean leaves. The parasitoid's basic search pathway consisted of walking, encountering the host, and drumming and probing it. While walking, the parasitoid stopped for short periods of time, partly to preen itself. Walking while searching comprised 61% of the adults' time budget and probing hosts represented 16%. After a host nymph was parasitized by A. fuscipennis , the parasitoid remained close by and continued searching for new hosts in the immediate vicinity. Such behaviour suggests area-restricted searching. The parasitoid preferred first instars of T. vaporariorum for oviposition, resulting in long developmental times. Amitus fuscipennis had a high percentage of host acceptance resulting in a high percentage parasitism (60%) of all encountered hosts. Amitus fuscipennis , on average, walked faster before an oviposition (1.4 mm/s) than other whitefly parasitoids. The implications of these findings for the control of T. vaporariorum are discussed.     

Host refuges and spatial patterns of parasitism in an endophytic host–parasitoid system

Abstract. 1. Larvae of Tephritis conura Loew (Diptera: Tephritidae) live gregariously in flower heads of Cirsium heterophyllum (L.) Hill (Cardueae). They are attacked by the endoparasitic wasps Eurytoma sp. near tibialis Boheman (Hymenoptera: Eurytomidae) and Pteromalus caudiger (Graham) (Hymenoptera: Pteromalidae).
2. The responses of the parasitoids to different host patch sizes were investigated from the analysis of field samples. At the host population level, overall probabilities of parasitism were independent of host numbers per flower head or showed a tendency to inverse density-dependence for both parasitoid species.
3. Measurements of ovipositor length in Eurytoma and P.caudiger indicated that parts of the flower head constitute a structural refuge from parasitism.
4. The accessibility of hosts in a flower head was found to differ markedly, depending on larval locations and flower head characters. In spite of this high variability, similar average percentages of larvae were accessible to the parasitoids in each patch size class.
5. High variability of oviposition success in laboratory experiments can be explained by random locations of hosts in the flower heads.     

Adult experience modifies attraction of the leafminer parasitoidOpius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals

Oviposition-experienced females of Opius dissitus Muesebeck, a braconid parasitoid of Liriomyza sativaeBlanchard, preferentially landed on leafminer-infested rather than uninfested lima bean (Phaseolus lunatus L.) plants in a flight tunnel assay. Both naive and oviposition-experiencedparasitoids responded strongly to odors of infested lima bean plants in a four-arm olfactometer in comparison with odors of uninfested plants, suggesting that volatile semiochemicals are used in host location. Parasitoids with an oviposition experience on lima bean (lima-experienced) spent significantly more time in the infested odor than naive individuals, however, eggplant-experienced wasps did not spend significantly more time in the infested odor field than naive wasps. When parasitoids reared on leafminers in lima bean were provided a choice between the odor of infested lima bean and the odor of infested eggplant or cotton, naive and lima-experienced wasps preferred infested lima odor. An oviposition experience on the other plant species resulted in a dramatic shift in preference. It was concluded that the experience effect was due, at least in part, to associative learning, as has been reported for other parasitoids. The parasitoids may perceive unconditioned stimuli during host contact and oviposition on an infested leaf and may associate those stimuli with volatile semiochemicals emanating from the leaf or host. Subsequently, the volatiles associated with the presence of hosts are used in directing the search for hosts.     

The influence of host distribution, sex, and size on the level of parasitism by Itoplectis conquisitor (Hymenoptera: Ichneumonidae)

Abstract. 1. Parasitism of the bagworm, Thyridopteryx ephemeraeformis Haw. (Lepidoptera: Psychidae), on red cedar was studied at Manassas, Va., U.S.A.
2. Fifteen parasitoids, five of which were hyperparasitoids, attacked the pupal stage of the bagworm. The Ichneumonid Itoplectis conquisitor alone accounted for 58% of the parasitized bagworms.
3. Parasitism by I conquisitor (Say) was inversely related to host size, but independent of host distribution within a tree. Male bagworms experienced disproportionately higher levels of parasitism than females. We conclude that it is small size that renders bagworms susceptible to parasitism rather than sex per se.
4. Ovipositor lengths of I.conquisitor were insufficient to penetrate the larger bagworm hosts (>57 mm); and in fact, as bagworm size increased, the proportion of the I.conquisitor population capable of penetrating the pupa declined abruptly. We suggest that the mechanical difficulties with oviposition, and perhaps the defensive capabilities of larger hosts, are responsible for the relationship between host size and per cent parasitism.
5. I.conquisitor could be an important selective agent for bagworm size at pupation, but it is not likely to act as a significant control agent of population density.     

Density dependence of Anaphes sordidatus (Hymenoptera: Mymaridae) parasitism on eggs of Listronotus oregonensis (Coleoptera: Curculionidae)

Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) oviposits in carrot leaves and the larvae feed in carrot roots. Its eggs are parasitized by Anaphes sordidatus (Girault) (Hymenoptera: Mymaridae) throughout its oviposition period. This parasitoid is the major biotic mortality factor for L. oregonensis. Parasitism by A. sordidatus was studied for three years in sequentially sown plots of carrots, Daucus carota var. sativa. Over the scason, significantly fewer L. oregonensis eggs were oviposited in later sown carrots than in earlier sown carrots because oviposition started later in late sown plots of carrots. A positive temporal density-dependent relationship was observed each year between parasitism rates and host densities. This positive density dependence occurred in early and mid-summer for earlysown carrots where host density reached 1–2 host eggs per plant but disappeared in late summer when host density decreased while parasitism remained high. Latesown carrots had low host egg density (0.2 host egg per plant) and contributed little to the total number of eggs. In these late sown plots, parasitism increased rapidly to over 80% but no density dependence was observed. Spatially, few statistically significant regressions were found but all indicated a positive spatial density-dependence. Most non-significant regressions occurred because the range of egg density was too small between plots for a given date.     

Gallery construction and oviposition of the bark beetle Ips typographus (Coleoptera: Scolytidae) at different breeding densities

Abstract. 1. The bole of a Norway spruce, Picea abies (L.) Karst., was cut in 25 cm sections and infested in the laboratory with 2 or 8 females/dm² of Ips typographus (L.) and an equal number of males.
2. One log of each beetle density was dissected every second day, beginning 2 days after female introduction.
3. The oviposition rate was highest at the beginning of the breeding period for both densities and then declined, especially at the high density. Residence time is a useful approximation for the number of laid eggs in the beginning of the oviposition period or when the density is low.
4. Final gallery length and egg number per gallery were on average significantly smaller at density 8 than at density 2.
5. Linear relationships between total gallery length and number of egg niches were found to be similar for the two densities.
6. An estimate of the egg to adult mortality at different densities was found by using data from a field study that related gallery length to breeding density in attacked living trees, together with published relationships between density and egg niches or emergence of new adults.
7. It was concluded that both decreased oviposition rate and earlier re-emergence at higher densities contribute to a declining oviposition with increasing density. The final offspring production is futher reduced by lower survival due to larval competition as density increases.     

Adaptive significance of facultative infanticide in the semi-solitary parasitoid Echthrodelphax fairchildii

Abstract.  1. This is the first work to show how imperfect kin recognition influences the behavioural strategy of parasitoids.
2. The female of Echthrodelphax fairchildii lays an egg on the right or left side of the host thorax. When superparasitising on the side without the first offspring, it often probed the opposite side with its sting and killed the first offspring more than 50% of the time. The frequency of probing increased with increasing inter-oviposition interval, and was higher in conspecific superparasitism than in self superparasitism.
3. The adaptiveness of probing was assessed by the difference in fitness returns between superparasitism with probing and superparasitism without probing. Fitness returns from self‐superparasitism and those from conspecific superparasitism were assessed by the fitness performance of both first and second comers, and that of second comers respectively.
4. In terms of the survival rate of immatures (one fitness component), probing under conspecific superparasitism guaranteed higher fitness returns than not probing for longer oviposition intervals, but under self‐superparasitism not probing guaranteed higher fitness returns for shorter intervals because superparasitism for such intervals often resulted in two-adult emergence.
5. In terms of head width (another fitness component), probing produced higher fitness returns for shorter oviposition intervals for both self and conspecific superparasitism.
6. Assuming that offspring quantity contributes more to fitness returns than does offspring quality, the observed frequencies of probing were considered adaptive for parasitoids whose abilities to distinguish between self and conspecifically parasitised hosts and to estimate inter-oviposition intervals are imperfect.     

Multitrophic influences on egg distribution in a specialized leaf beetle at multiple spatial scales

Egg distribution in herbivorous beetles can be affected by bottom-up (host plant), and by top-down factors (parasitoids and predators), as well as by other habitat parameters. The importance of bottom-up and top-down effects may change with spatial scale.

In this study, we investigated the influence of host plant factors and habitat structure on egg distribution in the leaf beetle Cassida canaliculata Laich. (Coleoptera: Chrysomelidae), a monophagous herbivore on Salvia pratensis L. (Lamiales: Lamiaceae), on four spatial scales: individual host plant, microhabitat, macrohabitat, and landscape. At the individual host plant scale we studied the correlation between egg clutch incidence and plant size and quality. On all other scales we analyzed the relationship between the egg clutch incidence of C. canaliculata and host plant percentage cover, host plant density, and the surrounding vegetation structure. Vegetation structure was examined as herbivores might escape egg parasitism by depositing their eggs on sites with vegetation factors unfavorable for host searching parasitoids.

The probability that egg clutches of C. canaliculata were present increased with an increasing size, percentage cover, and density of the host plant on three of the four spatial scales: individual host plant, microhabitat, and macrohabitat. There was no correlation between vegetation structure and egg clutch occurrence or parasitism on any spatial scale. A high percentage of egg clutches (38–56%) was parasitized by Foersterella reptans Nees (Hymenoptera: Tetracampidae), the only egg parasitoid, but there was no relationship between egg parasitism and the spatial distribution of egg clutches of C. canaliculata on any of the spatial scales investigated. However, we also discuss results from a further study, which revealed top-down effects on the larval stage.     

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.     

Trade-off in oviposition strategy: choosing poor quality host plants reduces mortality from natural enemies for a salt marsh planthopper

Abstract.  1. Both host plant nutrition and mortality from natural enemies have been predicted to significantly impact host plant selection and oviposition behaviour of phytophagous insects. It is unclear, however, if oviposition decisions maximise fitness.
2. This study examined whether the salt marsh planthopper Pissonotus quadripustulatus prefers higher quality host plants for oviposition, and if oviposition decisions are made so as to minimise mortality at the egg stage.
3. A controlled laboratory experiment and 4 years of field data were used to assess the rates of planthopper oviposition on higher quality 'green' and lower quality 'woody' stems of the host plant Borrichia frutescens . The numbers and percentages of healthy eggs and eggs that were killed by parasitoids or the host plant were recorded.
4. In all years, including the laboratory experiment, Pissonotus planthoppers laid more eggs on lower quality woody stems than on higher quality green stems. While host plant related egg mortality was higher in woody stems, the percentage of eggs parasitised was much greater in green stems. This resulted in a lower total mortality of eggs on woody stems.
5. The results of this study demonstrate that, although Pissonotus prefers lower quality host plants for oviposition, this actually increases fitness. These data seem to support the enemy free space hypothesis, and suggest that for phytophagous insects that experience the majority of mortality in the egg stage, oviposition choices may be made such that mortality is minimised.     

Physical and chemical plant characters inhibiting the searching behaviour of shape Trichogramma chilonis

Several plant characters are known to affect the searching behaviour and parasitization efficiency of Trichogramma spp. (Hymenoptera: Trichogrammatidae). In this study, plant characters contributing to the low Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) egg parasitism levels on pigeonpea (Cajanus cajan (L.) Millspaugh) were investigated. The efficiency of T. chilonis on pigeonpea was dependent on the plant structure on which the host eggs were found. In a cage experiment, more than 55% of eggs placed on leaves were parasitized, while 1% of eggs on calyxes and no eggs on pods were parasitized. In a filter paper bioassay, parasitoids were deterred by acetone and hexane surface extracts from pigeonpea pods but showed no response to water extract. The searching behaviour of the parasitoids was not affected by different solvent extracts from the surface of pigeonpea leaves. In a four-armed airflow olfactometer, T. chilonis was repelled by volatiles from pigeonpea pods but showed no response to volatiles derived from hexane extract of pod surfaces. Volatile infochemicals and hexane surface extracts from pods of two wild Cajanus species, C. scarabaeoides (L.) Thours and C. platycarpus (Bentham) van der Maesen, were similarly deterrent to T. chilonis. The movement of the parasitoids on pigeonpea pods and calyxes was inhibited by long trichomes and wasps were trapped by sticky trichome exudates. Parasitoids walked significantly faster on leaves than on pods. The walking speed on both pods and leaves increased significantly after washing with hexane. The results presented in this paper show that the plant growth stage and the plant structures preferred by H. armigera for oviposition are the least suitable for T. chilonis, contributing to the low parasitoid efficiency on pigeonpea.     

Influence of host density on the reproductive strategy of Cephalonomia stephanoderis, a parasitoid of the coffee berry borer

The effect of the density of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae) on reproductive and host-feeding behaviours of the parasitoid Cephalonomia stephanoderis (Hymenoptera: Bethylidae) was evaluated under laboratory conditions. The number of hosts used for oviposition was density-dependent at low host density. Beyond a density of six hosts/day, the oviposition rate reached a maximum of 1.2 eggs/day due to egg limitation. Cephalonomia stephanoderis females responded to increasing host availability with a linear increase in host feeding. Overall, parasitoids killed more coffee berry borers by feeding and paralysis than by parasitism. At low host density, the pre-oviposition phase was extended, oogenesis was delayed, more males were produced, and host feeding occasionally occurred concurrently with oviposition. We suggest that the efficacy of C. stephanoderis as a biological control agent depends on seasonal variations in host density. Inoculative vs inundative releases in coffee plantations are discussed in relation to the abundance of the coffee berry borer during the fructification and interharvest periods.     

Superparasitism as an ESS: to reject or not to reject, that is the question

A stochastic model is formulated to determine the optimal strategy for a solitary parasitoid which has discovered an already parasitized host. The model assumes that the parasitoid can count both the number of eggs already present in a host and the number of conspecifics searching in the same patch. The survival probability of an egg is assumed to depend on the total number of eggs in a host. The decision to (super)parasitize depends both on the degree to which the discovered host already is parasitized and on the number of conspecific females searching in the same patch. We consider both the case that egg laying does not involve any costs for the parasitoid and the case that it involves some marginal costs. Uniform behaviour of all the conspecific parasitoids in a patch, i.e. laying one additional egg in all encountered larvae containing a particular number of eggs, appears to be a pure evolutionary stable strategy (ESS). If either the probability that a parasitoid emerges from a host decreases with an increasing degree of parasitism, at least from a particular number of eggs onwards, or if parasitism involves marginal costs, the maximum number of eggs for which it is still profitable to superparasitize a host once more is limited. This number increases with the number of conspecifics searching in the patch. Large marginal costs (i.e. the expected gain of not parasitizing now) decrease the profit of superparasitism. For newly emerged parasitoids the rejection of an already parasitized host is not advantageous as long as the marginal costs of parasitism are small, because the host can never contain an egg of its own.