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.

     

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.     

The influence of insecticide residues on primary parasitoid and hyperparasitoid foraging behaviour in the laboratory

The behaviour of Aphidius rhopalosiphi DeStefani-Perez (Hymenoptera: Braconidae) was recorded in laboratory bioassays in the presence and absence of both residues of honeydew from the English grain aphid, Sitobion avenae (F.) and the pyrethroid insecticide, deltamethrin. Insecticide concentrations ranged from the field recommended dose rate (6.25 g ai/ha in 2001 water) to 1/16th of field rate. Parasitoids responded strongly to patches of honeydew on filter papers, however the addition of increasing concentrations of deltamethrin caused increasingly early departure from the honeydew-treated areas. Parasitoids pre-exposed to field concentration residues for between 1 and 20 min showed shorter retention times and abnormal types of behaviour on honeydew-treated patches compared to control wasps. Recovery of normal behaviour patterns occurred over a 12 h period away from the insecticide source. Further laboratory studies examined the foraging of A. rhopalosiphi and one of its associated hyperparasitoids, Dendrocerus carpenteri (Curtis), on mature wheat plants treated with an artificial honeydew solution and deltamethrin. Wasps exposed to deltamethrin residues were observed to spend shorter visit times, to groom more frequently and to rest less frequently than those on insecticide-free plants. Differences were found between the distribution of parasitoids on insecticide-treated and untreated plants, with D. carpenteri showing greater movement down insecticide-treated plants accompanied with an increase in time spent on abaxial leaf surfaces compared to A. rhopalosiphi. The results are discussed in terms of the repellency of deltamethrin and the implications for integrated pest management of differing sub-lethal insecticide effects on primary parasitoid and hyperparasitoid behaviour.     

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.     

Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality

Charnovs marginal value theorem predicts that female parasitoids should exploit patches of their hosts until their instantaneous rate of fitness gain reaches a marginal value. The consequences of this are that: (1) better patches should be exploited for a longer time; (2) as travel time between patches increases, so does the patch residence time; and (3) all exploited patches should be reduced to the same level of profitability. Patch residence time was measured in an egg parasitoid Anaphes victus (Hymenoptera: Mymaridae) when patch quality and travel time, approximated here as an increased delay between emergence and patch exploitation, varied. As predicted, females stayed longer when patch quality and travel time increased. However, the marginal value of fitness gain when females left the patch increased with patch quality and decreased with travel time. A. victus females appear to base their patch quality estimate on the first patch encountered rather than on a fixed innate estimate, as was shown for another egg parasitoid Trichogramma brassicae. Such a strategy could be optimal when inter-generational variability in patch quality is high and within-generational variability is low.     

Interpatch movement of the red milkweed beetle,Tetraopes tetraophthalmus: individual responses to patch size and isolation

Individual movement patterns and the effects of host plant patch size and isolation on patch occupancy were examined for red milkweed beetles, Tetraopes tetraophthalmus, residing in a heterogeneous landscape. Male beetles were found to move both more often and farther between host plant patches than female beetles, and this difference affected the patterns of patch occupancy observed. Overall, unoccupied milkweed patches were smaller and more isolated than patches occupied by beetles. Patches uninhabited by females tended to be more isolated, but not necessarily smaller, than patches with female beetles, indicating that females may be affected more by patch isolation than patch size. Presence of male beetles on patches showed a stronger response to patch size than to patch isolation. Differences in movement between males and females illustrate the need for demographically based dispersal data. Comparisons of Tetraopes interpatch movement patterns between landscapes composed of patches of different size revealed that landscapes with overall smaller patches may have greater rates of interpatch movement.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

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.     

Patch occupancy in the endangered butterfly Lycaena helle in a fragmented landscape: effects of habitat quality, patch size and isolation

While there is agreement that both habitat quality and habitat network characteristics (such as patch size and isolation) contribute to the occupancy of patches by any given species, the relative importance of these factors is under debate. This issue is of fundamental ecological importance, and moreover of special concern for conservation biologists aiming at preserving endangered species. Against this background we investigated patch occupancy in the violet copper Lycaena helle, one of the rarest butterfly species in Central Europe, in the Westerwald area (Rhineland-Palatinate, Western Germany). Occupied (n = 102) differed from vacant (n = 128) patches in altitude, size, connectivity, availability of wind shelter, in the abundance of the larval host-plant, in the abundance of a grass species indicating favorable habitat conditions and in the abundance of nitrophilous plants. Overall, patch occupancy was primarily determined by patch size, connectivity and the abundance of the larval host plant, while all other parameters of habitat quality were of subordinate importance. Therefore, our findings suggest that even for extremely sedentary species such as L. helle habitat networks are decisive and—next to the preservation of habitat quality—need to be an integral part of any conservation management for this species.     

Patch clamp study of the voltage-dependent anion channel in the thylakoid membrane

Measurements of single channel currents were performed on isolated membrane patches from osmotically swollen thylakoids of the Charophyte alga Nitellopsis obtusa. A channel with a high selectivity for anions over cations and a conductance of 100 to 110 pS (114 mM Cl–) was revealed. The channel has a bells-haped voltage-dependence of the open probability, with a maximum at about 0 mV. This dependence was explained by two gating processes, one causing channel closure at positive and one at negative potentials. The steepness of the voltage-dependence corresponded to approximately 2 elementary charges to be transferred across the entire membrane in each of the two gating processes. The analysis of the anion channel kinetics in the millisecond time domain revealed an e-fold increase of mean open and decrease of mean closed times when the membrane voltage was made more positive by 20 and 36 mV, respectively. Concert transitions of two identical anion channels between open and long inactivated states were observed, while the millisecond closed-open transitions of the two channels within a burst of activity were kinetically independent.This work was financially supported by the Deutsche Forschungsgemeinschaft (SFB 176 TP B11) and by a research fellowship from the Alexander von Humboldt Foundation to I.I. Pottosin.     

Sex pheromones in the cereal aphid parasitoidsPraon volucre andAphidius rhopalosiphi

Laboratory and field experiments provided evidence for the release of sex pheromones by virgin femalePraon volucre Haliday andAphidius rhopalosiphi De Stefani-Perez (Hymenoptera: Braconidae, Aphidiinae). In Petri dish biosassays, rubber or vermiculite models treated with crude virgin female extracts were frequently approached by males and elicited rapid wing-fanning behaviour and copulation attempts. Delta-shaped water traps containing live virgin females caught large numbers of conspecific males when placed in winter wheat crops. Trapping slightly below crop height resulted in higher catches than trapping above the crop canopy.     

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.     

Host discrimination and evidence for a host marking pheromone in the almond seed wasp, Eurytoma amygdali

Laboratory experiments and observations on the oviposition behaviour of the almond seed wasp Eurytoma amygdali Enderlein (Hymenoptera, Eurytomidae) revealed that the females of this species deposit a host-marking pheromone, immediately after an oviposition, by dragging the tip of their abdomen on the fruit surface. This pheromone enables them to discriminate between the infested and uninfested fruit and to select for oviposition the latter. Its primary function is apparently the prevention of repeated ovipositions in already infested fruit, thus contributing to the optimal utilisation of the available resources for larval development. The responses of individual females to different treatments of almonds, in a series of two-choice tests, revealed that the pheromone can be perceived by the females on direct contact and, when at high concentrations, also olfactorily from a short distance. The pheromone was present inside the abdomen and thorax of females but not of males, and, although water soluble, could not be entirely removed from heavily infested almonds when rinsed with water. Direct observations revealed that after an average of 3.7 successive visits to pheromone-bearing almonds, females were induced to walk or, most often, fly away from the experimental set-up. This suggests that the pheromone may also contribute to the dispersion of the wasps.

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Résumé Des expériences de laboratoire et des observations concernant le comportement de ponte de Eurytoma amygdali Enderlein (Hymenoptera, Eurytomidae) ont montré que, immédiatement après la ponte, les femelles déposent une phéromone de marquage de l'hôte en trainant le bout de leur abdomen sur la surface de l'amande. Cette phéromone les rends capable de distinguer les fruits infectés des non-infectés dt de sélectionner pour la ponte les derniers. Apparemment, la fonction principale de cette phéromone est la prévention de la répétition des ovipositions dans les fruits déjà infectés et la répartition uniforme des oeufs dans les amandes, contribuant ainsi à la meilleure utilisation des ressources disponsibles pour le développement des larves. Des expériences de deux choix entre des fruits de différents traitements ont montré que la phéromone pouvait être perçue par les femelles par le direct contact et, quand elle était à hautes concentrations, par olfaction d'une courte distance. La phéromone était présente dans l'abdomen et dans le thorax des femelles, et bien qu'elle soit soluble à l'eau, elle ne pouvait pas s'éloigner entièrement par lavage des amandes sérieusement infectées à l'eau. Les observations ont démontré qu'après un numéro de 3.7 visites successives sur des amandes portant de la phéromone les femelles s'éloignaient du lieu de ponte en marchant ou, le plus souvant, en s'envolant, ce qui suggère que la phéromone contribue à la dispersion des femelles.

     

Catching Ariadne by her thread: how a parasitoid exploits the herbivore's marking trails to locate its host

Chemical signals that can be associated with the presence of a host insect often work as arrestants in close range host location by parasitoids, leading to longer searching times on patches where such signals are present. Our current view of parasitoid host location is that by prolonging the search times in patches, randomly searching parasitoids enhance their chance of detecting host insects. However, prolonged search times are not necessarily the only modification in parasitoid behaviour. In this study, we examine the exploitation of host-fruit marking pheromone of rose-hip flies, Rhagoletis basiolaOsten-Sacken (Diptera: Tephritidae) by the specialized egg-larval parasitoid Halticoptera rosae Burks (Hymenoptera: Pteromalidae). We provide evidence that the instantaneous probability that a host egg will be located by a searching parasitoid wasp differs markedly between pheromone-marked and unmarked fruits. The arresting response to the marking pheromone, i.e., the prolonged time a wasp is willing to search on marked fruits, can only account for a small fraction of the difference in successful host location on marked and unmarked fruits. We further demonstrate that the time wasps require to locate the host egg is independent of the size of the rose-hip harbouring the fly egg, and thus is independent of the area the wasp potentially has to search. A comparison of our findings with results of different search algorithms for parasitoid wasps suggests that wasps use the fly's pheromone marking trail as a guide way to the fly's oviposition site and thus the host egg.     

Functional significance of the alarm pheromone composition in various morphs of the green peach aphid, Myzus persicae

Three isomers of farnesene occur in the siphon excretions of at least four aphid species: the siphon excretions of Myzus persicae contain (E)--farnesene, as well as (Z,E)--farnesene. The significance of (E)--farnesene as an alarm pheromone was evaluated by the investigation of the ratios and quantities of the above-mentioned farnesene isomers in various morphs of Myzus persicae (Sulz.). It is suggested that a relationship exists between the production of farnesene isomers and the occurrence of morphs.

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Zusammenfassung Es ist bekannt, dass drei Isomere des Farnesens in der Siphonensekret von wenigstens vier Blattläusmorphen vorkommen. So enthielt zum Beispiel das Siphonensekret bei Myzus persicae (E)--, (Z,E)-- und (E,E)--Farnesen. Um die Bedeutung des (E)--Farnesens zu ermitteln, haben wir die Mengen und Verhältnisse der Farnesenisomere in verschiedenen Morphen von Myzus persicae bestimmt. Die Ergebnisse deuten darauf hin, dass eine Beziehung zwischen der Produktion von Farnesenisomeren und der Bildung der Morphe in dieser Blattläus besteht.

     

Patch selection by red deer in relation to energy and protein intake: a re-evaluation of Langvatn and Hanley's (1993) results

Langvatn and Hanley (1993) recently reported that patch use by red deer (Cervus elaphus) was more strongly correlated with short term rates of intake of digestible protein than dry matter. Such short term measures overlook effects of gut filling, which may constrain intake by ruminants over longer time scales (i.e., daily rates of gain). We reanalyzed Langvatn and Hanley's data using an energy intake model incorporating such a processing constraint, to determine whether their conclusions are robust. We found that the use of patches by red deer was just as strongly correlated with an estimate of the daily rate of intake of digestible energy as one of digestible protein during four out of seven trials, but slightly lower in three out of seven trials. In all cases, daily intake of digestible energy was a much better predictor of patch preference by red deer than was the intake of dry matter. Our reanalysis suggests that the daily intake of energy was highly correlated with that of protein in these trials, as may often be the case for herbivores feeding on graminoids. Hence the observed pattern of patch use by red deer could simultaneously enhance rates of both protein and energy intake.     

Survey of the parasitoids of the tuliptree aphid,Illinoia liriodendri (Hom: Aphididae), in northern California

A survey of the parasitoids ofIllinoia liriodendri (Monell) in northern California conducted from 1988–1990 revealed the presence of 12 primary and 14 hyper-parasitoid species. The most common primary parasitoid wasAphidius polygonaphis (Fitch), which was imported from the eastern United States in the 1970's and is now established throughout the area. New host records were noted forA. ervi Haliday,A. avenaphis (Fitch), Praon occidentale Baker,P. unicum Smith,Diaeretiella rapae M'Intosh,Lysiphlebus testaceipes (Cresson), andMonoctonus nervosus (Haliday) (all Hymenoptera: Braconidae: Aphidiinae), andAphelinus sp. nr.asychis Walker (Hymenoptera: Aphelinidae). The most common hyperparasitoid species werePachyneuron aphidis (Bouché) andAsaphes californicus Girault (both Hymenoptera: Pteromalidae). New hyperparasitoid host records were noted forPachyneuron californicum Girault on Aphidiine and Aphelinidae spp. andCoruna clavata Walker (Hymenoptera: Pteromalidae) onAphelinus sp.     

Colony orientation and successful defence behaviour in the conifer aphid, Schizolachnus pineti

We studied colony structure and body orientation behaviour of Schizolachnus pineti, a specialised aphid feeding on needles of Scots pine. Aphids feeding at the margin of a colony always face towards the centre of the colony, bounding the colony with their legs. This behaviour increased the defence success aginst the specialised parasitoid (Pauesia unilachni) and the specialised predator (Scymnus nigrinus). Both enemies had less success when attacking S. pineti from the abdominal site when compared to the front. We assume that the defence orientation displayed by marginally feeding aphids has an adaptive nature and is particularly effective when feeding in a row on linear plant structures such as needles.