Nocturnal activity and resource utilization in the aphid hyperparasitoid, Dendrocerus carpenteri

Abstract.

• 1 Females of the aphid hyperparasitoid Dendrocerus carpenteri (Curtis) search successfully for hosts during both day and night. Oviposition numbers per host patch did not differ significantly between day and night.
• 2 D.carpenteri females also displayed a nocturnal flight activity, showing that they are not only capable of searching on a given host plant but also of dispersing between host plants.
• 3 Nocturnal oviposition activity was mainly influenced by egg load. Females with a high egg load laid more eggs at night than females with a comparatively low egg load. Thus, D.carpenteri females may use nocturnal foraging to compensate for the lack of oviposition opportunities during day.
• 4 D.carpenteri females which foraged continuously for hosts both day and night (= for 24 h per day) benefitted from an 1.4-fold increase in lifetime reproductive success when compared to females which foraged only by day (= for 16 h per day).
• 5 The benefit of night foraging for this species is a significantly increased reproductive success.

     

Foraging for mates in the hyperparasitic wasp, Dendrocerus carpenteri: impact of unfavourable weather conditions and parasitoid age

Males of the aphid hyperparasitoid Dendrocerus carpenteri (Curtis) were attracted by a sex pheromone released by conspecific females. The intensity of this cue, and thus female attractiveness, depended both on the female's mating status and her age. Only virgin females younger than 2 h were consistently recognized as mates by foraging males. Male age did not influence foraging and mating success. Empty mummies, from which females had emerged within the previous 10 min were attractive to males and examined intensively. Rain reduced the searching success of males, although the host plant Vicia faba provided sheltered places. Wind did not reduce mating success but prevented both sexes from leaving the host plant. Since the time of female attractiveness seems to be very limited, wind may have an enormous effect on the mating success of D. carpenteri in the field and thus on the population dynamics of this species. Received: 5 October 1998 / Accepted: 16 December 1998     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non-significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.     

Flexible use of patch marks in an insect predator: effect of sex, hunger state, and patch quality

Abstract 1. Patch marks that allow the subsequent avoidance of marked areas may be used by small animals to increase foraging efficiency. This study is the first to demonstrate the presence of a patch-marking system in insect predators. Furthermore, the marking system is found only in females, and factors such as hunger state and patch quality play a key role in determining whether a female will re-investigate a self-marked patch.
2. Females of the insect predator Orius sauteri avoided areas where the female itself had searched previously but did not avoid areas searched by conspecific females when deprived of prey for 24 h . There was no evidence that males use such a patch-marking system, indicating the presence of a sex difference in patch-mark use.
3. Females did not discriminate between patches visited previously and patches not visited when they were either well fed or when patches contained abundant prey.
4. The patch mark used by females was effective for ≤ 1 h and may be a reliable indicator of a recently visited area in which prey have been depleted.
5. These results suggest that O. sauteri females have the flexibility to adjust their behavioural responses to a previously searched area depending on their hunger state and the availability of prey in their foraging environment.     

Age and experience influence patch assessment for oviposition by an insect predator

Abstract.  1. Dynamic models of optimal foraging predict that an animal's decision to accept or reject a patch depends not only on the environment and patch quality, but also on its internal state. Previous experiments have shown that the two-spot ladybird beetle, Adalia bipunctata (L.), is reluctant to lay eggs in a patch of prey contaminated by the oviposition-deterring pheromone produced by conspecific larvae.
2. An experiment was conducted to test whether the internal state of an A. bipunctata female affects its oviposition response to oviposition-deterring pheromone. Firstly, the oviposition response to oviposition-deterring pheromone of young and old females was compared. Secondly, the oviposition response to oviposition-deterring pheromone of females previously exposed continuously to oviposition-deterring pheromone was compared with that of females of the same age but with no previous experience of oviposition-deterring pheromone.
3. Old females and females with previous experience of oviposition-deterring pheromone were less reluctant to lay eggs in the presence of oviposition-deterring pheromone than young and naive females. These results are consistent with the predictions of optimal foraging theory.     

Competition for hosts between two hyperparasitoids of aphids,Dendrocerus laticeps andDendrocerus carpenteri (Hymenoptera: Megaspilidae): The benefit of interspecific host discrimination

The two hyperparasitoids of aphids, Dendrocerus carpenteri(Curtis) and Dendrocerus laticeps(Hedicke), differ in their interspecific host discrimination behavior: D. carpenterireadily accepts hosts for oviposition previously parasitized by D. laticeps,whereas D. laticepsoften refrains from ovipositing on hosts previously parasitized by D. carpenteri.The two species also differ in their competitive abilities: D. carpenteriis competitively superior to D. laticepswhen the time between ovipositions is 1 h. D. carpenteri's superiority probably arises from (a) the action of the venom produced by the female to paralyze the host, as evidenced by the comparison of emergence patterns from naturally vs artificially parasitized hosts, and (b) its more rapid egg development. Because of its competitive abilities, D. carpenterigains only limited benefit from discriminating interspecifically, at least when encountering a host parasitized by a competitively inferior species, such as D. laticeps.In contrast, D. laticepsgains considerable benefit from recognizing hosts previously parasitized by D. carpenteri,as the probability to produce offspring from such hosts is greatly reduced.     

Self and conspecific superparasitism by the solitary parasitoid Antrocephalus pandens

Abstract.

• 1 The fitness consequences of superparasitism for a solitary parasitoid depend on whether the host was first parasitized by itself (‘self-superparasitism’) or a different individual (‘conspecific superparasitism’). Self superparasitism is usually expected to be avoided.
• 2 A.pandens females showed no difference in their probability of superparasitism between self-parasitized and conspecifically-parasitized hosts. The probability of superparasitism decreased as time from the laying of the first egg in a host increased, from about 0.29–0.46 at a time interval of 1 h to 0.10–0.14 at 72 h.
• 3 The egg distribution of wasps foraging alone on a patch showed significant avoidance of superparasitism, but that of wasps foraging in the presence of conspecifics was not significantly different from a random distribution. This suggests that wasps switch from avoidance of superparasitism when alone to acceptance of all hosts when in a group.
• 4 When wasps foraged in a group, the hosts had many more ovipositor puncture marks than when wasps foraged singly. This suggests that either hosts were attacked several times per encounter, or that the wasps' encounter rate with hosts was much higher when in a group. If the latter is true, it is possible that, although the egg distribution suggested a higher rate of superparasitism when wasps foraged in a group, the ratio of acceptances to contacts of parasitized hosts may in fact have been lower.

     

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.     

Superparasitism in the solitary ectoparasitoid Aptesis nigrocincta: the influence of egg load and host encounter rate

Theory predicts that the acceptance of hosts already parasitized by a conspecific will depend both on egg load and the availability of hosts. In the present laboratory study, we tested the effect of egg load and host encounter rate on the propensity of superparasitism in the solitary parasitoid Aptesis nigrocincta Gravenhorst (Hymenoptera, Ichneumonidae), a synovigeneous ectoparasitoid of prepupae of the European Apple Sawfly. Parasitoid females carry few voluminous eggs at a time and the egg maturation rate is less than one egg per day. Egg load was manipulated by giving females access to hosts one week prior to the start of treatments and host availability by giving females access to either one host cocoon every day or every other day. In the first treatment where females had a high egg load of 5.3 egg in their ovaries and encountered host cocoons at low rates, we found that parasitized hosts were accepted to the same degree as healthy hosts. In females with significantly decreased egg load (3.8 eggs) encountering hosts at the same rate we found a slight but non‐significant decrease in the acceptance of parasitized hosts compared with healthy hosts. In contrast, A. nigrocincta females accepted significantly fewer parasitized hosts at a high host encounter rate that would lead them to the point of egg limitation in the near future. Within the range of egg loads tested, the host encounter rate appears to be the most important determinant for a females decision to oviposit onto hosts already parasitized by a conspecific.     

Influence of host distribution on foraging behaviour in the hyperparasitoid wasp, Dendrocerus carpenteri

The foraging behaviour of Dendrocerus carpenteriCurtis (Hymenoptera: Megaspilidae), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids, was examined in the laboratory with an experimental system consisting of broad bean, Vicia fabaL, the pea aphid, Acyrthosiphon pisumHarris, and a primary parasitoid, Ephedrus californicusBaker. Pea aphids parasitised by E. californicusoften disperse from their feeding sites (or off host plants) before dying and mummifying. Response of female hyperparasitoids to host distribution was evaluated at two spatial scales. At the first scale, behaviour of hyperparasitoids was examined on individual plants with different densities of hosts. At the second scale, habitat complexity and host location were manipulated in large foraging cages containing several plants. I show that patterns of density-dependent hyperparasitism can result from the foraging behaviour of D. carpenteri. However, dispersal of parasitised aphids may not reduce the incidence of hyperparasitism if hyperparasitoids systematically search the habitat.     

Assessment of patch quality by ladybirds: role of larval tracks

Gravid females of the two-spot ladybird, Adalia bipunctata (L.), were deterred from ovipositing when kept in petri dishes that had previously contained conspecific larvae but not conspecific adults, or the larvae of another two species of ladybird, Adalia decempunctata (L.) and Coccinella septempunctata L. The deterrent effect was density dependent and mediated via a chloroform-soluble contact pheromone present in the larval tracks. Similarly, gravid females of C. septempunctata were deterred from ovipositing by conspecific larval tracks and chloroform extracts of these tracks, but not by the tracks or extracts of tracks of A. bipunctata larvae. That is, in ladybirds the larvae produce a species-specific oviposition-deterring pheromone. In the field, the incidence of egg cannibalism in ladybirds increases very rapidly with the density of conspecific eggs or larvae per unit area. Thus, in responding to the species specific oviposition deterring pheromone female ladybirds reduce the risk of their eggs being eaten and spread their offspring more equally between patches. Received: 14 March 1997 / Accepted: 26 August 1997     

Unrewarding experiences and their effect on foraging in the parasitic waspLeptopilina heterotoma (Hymenoptera: Eucoilidae)

The host-foraging behavior of female entomophagous parasitoids is commonly modified by positive associative learning. Typically, a rewarding experience (e.g., successful oviposition in a host) increases a female's foraging effort in a host microhabitat of the type associated with that experience. Less well understood are the effects of unrewarding experiences (i.e., unsuccessful foraging). The influence of unrewarding experience on microhabitat choice and residence time within a microhabitat was examined for the eucoilid parasitoid,Leptopilina heterotoma, in laboratory and greenhouse assays. As determined previously, females which oviposited successfully in either of two microhabitat types (fermenting apple or decaying mushroom) strongly preferred to forage subsequently on that microhabitat type. However, failure to find hosts in the formerly rewarding microhabitat caused females to reverse their preference in favor of a novel microhabitat type. The effect, though striking, was transient: within 1–2 h, the original learned preference was nearly fully restored. Similar effects of unrewarding experiences were observed with respect to the length of time spent foraging in a microhabitat. As determined previously, oviposition experience in a particular microhabitat type increased the time spent foraging in a patch of that microhabitat type. However, failure to find hosts in the patch caused the time a wasp spent in the next unoccupied patch of that type to decrease to almost nothing. In addition, there was a tendency for an unrewarding experience on a formerly rewarding microhabitat type to extend the time spent in a patch of a novel type. The function of the observed effects of unrewarding experiences is discussed.     

Presence of a conspecific increases superparasitism but not infanticide under self‐ and conspecific superparasitism in a semisolitary parasitoid,Echthrodelphax fairchildii (Hymenoptera: Dryinidae)

Female parasitoids are expected to avoid superparasitism (ovipositing in and/or on parasitized hosts) when unparasitized hosts are available. However, when the supply of unparasitized hosts is restricted, they are expected to self‐ as well as conspecifically superparasitize. One of the cues of a reduced availability of unparasitized hosts is the presence of a conspecific. Moreover, if the focal species can perform infanticide, after encountering a conspecific female, the females are expected to kill eggs existing in and/or on hosts when superparasitizing, because the eggs are more likely to be laid by others. In this study we investigated whether females of an infanticidal semisolitary parasitoid, Echthrodelphax fairchildii, increase their frequencies of superparasitism and infanticide after encountering a conspecific female. Echthrodelphax fairchildii females are capable of discriminating between self‐ and conspecific superparasitism until up to 0.75 h after the first egg was laid (self‐superparasitism frequency < conspecific superparasitism frequency). As expected, the female parasitoids were more likely to perform self‐ and conspecific superparasitism after they had encountered a conspecific. In particular, the self‐superparasitism frequency increased highly within a short period after the first oviposition, so that no difference between the self‐ and conspecific superparasitism frequencies was found. In contrast, the infanticidal‐probing frequency remained extremely low, irrespective of whether or not the female parasitoids had encountered a conspecific. Moreover, when superparasitizing, females usually laid female eggs. Possible causes for the low frequency of infanticidal probing and the female‐biased sex ratio are discussed.     

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.     

Prey Habitat Location by the Cassava Mealybug Predator Exochomus flaviventris: Olfactory Responses to Odor of Plant, Mealybug, Plant–Mealybug Complex, and Plant–Mealybug–Natural Enemy Complex

Exochomus flaviventris Mader is considered to be the most active predator of the cassava mealybug Phenacoccus manihoti Matile–Ferrero in Central Africa. The response of experienced gravid female coccinellids to the odor of cassava plant (var. Zanaga), unparasitized mealybugs, plant–mealybug complex with or without feeding prey (parasitized or not), and plant–mealybug complex with or without conspecific coccinellids was investigated in a Y-tube olfactometer. The odor of uninfested cassava plants was not more attractive than clean air. Dual-choice tests revealed that mealybug-infested plants were preferred to mealybugs alone and mealybug-damaged plants and were the major sources of volatiles that attract females coccinellids to the microhabitat of its prey. The emission of volatile chemicals did not appear to be limited to the infested parts of the plant but did occur systemically throughout the plant. The presence of conspecific coccinellid larvae or adult males did not modify the attractiveness of the mealybug-infested plants. However, when an infested plant with conspecific predator females (alone or with conspecific males) was compared to an infested plant or infested plant with conspecific males, E. flaviventris females showed a preference for the last two sources of odor. The uninfested plant with conspecific males was also preferred to the uninfested plant with conspecific females. In addition, the odor of conspecific males was preferred over that of conspecific females. Female predators preferred the plant infested with unparasitized mealybugs over the plant infested with mealybugs previously parasitized. These results showed that E. flaviventris females use herbivore-induced plant volatiles during foraging and can detect via olfaction the presence of conspecific gravid females and parasitized prey, thus assessing patch suitability from a distance.     

Facilitation in Ovipositional Behavior of Bactrocera tryoni Flies

Mature female Queensland fruit flies, Bactrocera tryoni Froggatt, released into canopies of field-caged trees containing host fruit, did not discriminate between fruit having or lacking two resident conspecific females when selecting fruit on which to alight. When released individually onto a fruit, mature females showed no greater or lesser propensity to initiate boring with the ovipositor into fruit having or lacking a resident female engaged in pre-ovipositional or post-ovipositional behavior. However, boring propensity of introduced females was significantly enhanced or facilitated when released onto fruit on which a conspecific female was in the act of ovipositing. Introduced females were significantly more prone to initiate boring into high-ranking fruit (nectarines) than low-ranking fruit (lemons) and to do so when having a high rather than a low egg load. Neither fruit type nor egg load of introduced females had a significant effect on the occurrence of encounters between introduced and resident females, on the occurrence of contests, or on the propensity of introduced females to initiate boring in the presence of a resident female. Among introduced females, there was a consistent trend to initiate boring earlier in the presence than in the absence of a resident female. We discuss circumstances, likely to be narrow, under which boring propensity of an intruding female might be facilitated in the presence of a resident female.     

Evidence for a marking pheromone in host discrimination byCephalonomia Stephanoderis (Hym.: Bethylidae)

The bethylidCephalonomia stephanoderis Betrem is an ectoparasitoid that prefers to oviposit on the prepupae and pupae of the coffe berry borerHypothenemus hampei (Ferrari) (Coleoptera: Scolytidae). It has the ability to distinguish unparasitized from parasitized hosts and rarely lays more than one egg per host. The mechanism of this host discrimination byC. stephanoderis was investigated under laboratory conditions. For this, parasitoid eggs that had been deposited on host pupae were removed and pupae were then offered (individually and collectively) to individual female wasps. A total of 92% of individually offered hosts and 93% of collectively offered hosts were not parasitized. It is concluded thatC. stephanoderis recognizes a marking pheromone deposited into or onto the host, preceding, during, or after oviposition which enables female parasitoids to avoid self and conspecific superparasitism.     

Sex-allocation behaviour of a solitary ectoparasitoid: effects of host-patch characteristics and female density

The sex-allocation behaviour of the solitary ectoparasitoid Dinarmus basalis (Hymenoptera: Pteromalidae) was investigated by examining the female's response to two proximal factors: the host-patch characteristics and the conspecific female density in the patch. The offspring sex-ratio of single females presented with unparasitised hosts was female biased (approximately three daughters to one son in the progeny) whatever the host density tested. The sex-ratio in the presence of hosts parasitised by a conspecific 48 h beforehand was male biased. The proportion of male offspring also increased when the number of conspecific females exploiting the patch changed from a single female to a group of females, whatever the group size. No sexual differences in mortality as a result of larval competition on superparasitised hosts were observed. The offspring sex-ratios observed in response to the host-patch characteristics were the result of manipulation of the egg fertilisation by the females during the oviposition phase. Thus, the variability of the sex-ratio in response to an increase in the number of conspecific females in the same patch represented a reduction in egg fertilisation. These results are analysed with regard to the predictions of Local Mate Competition theory and the females' host discrimination ability.     

Host-feeding and acceptance by a parasitic wasp (Hymenoptera: Ichneumonidae) as influenced by egg load and experience in a patch

Optimal host selection models based on dynamic programming predict that the physiological state of a foraging insect, i.e. egg load, energy reserves etc., influences behavioral decisions. To test this prediction, the effect of physiological state on host acceptance of the ectoparasitic wasp Agrothereutes lanceolatus was investigated. Female wasps in plastic cups (regarded as patches) were presented with hosts, and their responses to the hosts were continuously observed. After observations, the wasps were dissected and the number of mature and immature eggs they carried were counted. The results showed that behavioral decisions by the female wasps were influenced by mature egg load, but not by wasp size or immature egg load. Hence the wasps with higher egg loads were more likely to oviposit. The number of hosts previously encountered in a patch (i.e. wasp experience) also had an independent effect on females' host acceptance, indicating that female informational state was updated during foraging in that patch. Female wasps host-fed only when mature egg load approached zero. Concurrent host-feeding was not observed. Parasitoid survival was almost zero when parasitoid eggs were transferred onto hosts that were fed upon, indicating that concurrent host-feeding could cause a high degree of offspring mortality. These three results supported the assumption and prediction of optimal host-feeding models. Parasitoid host selection and host-feeding are discussed in the context of recent models.     

Egg laying rather than host quality or host feeding experience drives habitat estimation in the parasitic wasp Nasonia vitripennis

In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences—such as ample time to investigate hosts, host feeding, or egg laying—would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.