Foraging behaviour of the parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae) in response to plant volatiles,with reference to biocontrol of aphids in peri-urban vegetable production systems

Foraging behaviour of Lysiphlebus testaceipes was studied in a Y-tube olfactometer. Naïve females responded to the Aphis gossypii/eggplant complex on which they had been reared, but did not show a preference for this aphid/plant complex over an uninfested eggplant, an eggplant that had been damaged by the aphid or an A. gossypii/okra complex. Females that had been allowed to forage on the A. gossypii/eggplant complex before being tested in the olfactometer showed a strong preference for an uninfested eggplant over an uninfested okra plant and for the A. gossypii/eggplant complex over an A. gossypii/okra complex, indicating that they had learned to associate eggplant-derived volatiles with host availability. When females that had been reared on the A. gossypii/eggplant complex were tested after foraging experience on the A. gossypii/okra complex, they did not show a preference for either complex, suggesting that they still retained a memory of the cues associated with the complex on which they had been reared. The efficiency of L. testaceipes as a biological control agent in peri-urban vegetable production, such as the Cuban organoponics system, potentially could be improved by producing and releasing females behaviourally primed to prefer specific host/plant complexes.     

Microsatellite DNA markers for Lysiphlebus testaceipes

Microsatellite loci were isolated from the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae). Ten loci were obtained from an enriched partial genomic library. Genetic diversity was analysed at seven of these loci and two natural populations, one on oleander and one on citrus. The observed number of alleles ranged from one to 17, and the observed heterozygosity ranged from 0.37 to 0.82. In both populations, no departure from Hardy–Weinberg equilibrium was detected except for one locus. The differentiation between the two populations was characterized by an F_ST of 0.09.     

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

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

Contagious parthenogenesis, automixis, and a sex determination meltdown

Because of the twofold cost of sex, genes conferring asexual reproduction are expected to spread rapidly in sexual populations. However, in reality this simple prediction is often confounded by several complications observed in natural systems. Motivated by recent findings in the Cape honey bee and in the parasitoid wasp Lysiphlebus fabarum, we explore through mathematical models the spread of a recessive, parthenogenesis inducing allele in a haplodiploid population. The focus of these models is on the intricate interactions between the mode of parthenogenesis induction through automixis and complementary sex determination (CSD) systems. These interactions may result in asexual production of diploid male offspring and the spread of the parthenogenesis-inducing allele through these males. We demonstrate that if parthenogenetic females produce a substantial proportion of male offspring, this may prevent the parthenogenesis-inducing allele from spreading. However, this effect is weakened if these diploid males are at least partially fertile. We also predict a degradation of multilocus CSD systems during the spread of parthenogenesis, following which only a single polymorphic CSD locus is maintained. Finally, based on empirical parameter estimates from L. fabarum we predict that male production in parthenogens is unlikely to prevent the eventual loss of sexual reproduction in this system.     

Microsatellite-based parentage analysis reveals non-ideal free distribution in a parasitoid population

Habitat selection by dispersers is the focus of much theoretical models, most of which are based on the assumption of negative density dependence. The archetype of these models is the ideal free distribution, characterized by an evolutionary stable state where more competitors aggregate in better habitats, so that the fitness benefit of resource abundance is equally offset by the cost of competition in all habitats. In this study, we used parentage analysis on microsatellite genotypes to test the ideal free distribution in a natural population of aphid parasitoids. Parentage analysis was conducted on parasitoids emerging from aphid colonies. We inferred the number of foundress females which had reproduced in each colony, as well as the number of offspring for each foundress. As predicted by the ideal free distribution, the number of offspring per foundress per colony did not depend on the number of hosts per colony. However, contrary to ideal free distribution predictions, it was affected by the number of foundresses per colony. In surprising contrast with the basic assumption of negative density dependence, individual fitness increased with the number of foundresses. Moreover, parentage analysis revealed a very low number of offspring per foundress per colony (mean = 1.8). This observed distribution questions the validity of classical models of habitat choice based on competition. Indeed, our results provide a new illustration reinforcing a growing body of theory and data on positive density dependence. Our results also suggest that the avoidance of hyperparasitism and predation, although generally neglected, may shape the distribution of parasitoids in the field.     

MOLECULAR MARKERS INDICATE RARE SEX IN A PREDOMINANTLY ASEXUAL PARASITOID WASP

The parasitoid wasp genus Lysiphlebus (Hymenoptera: Braconidae: Aphidiinae) contains a taxonomically poorly resolved group of both sexual (arrhenotokous) species and asexual (thelytokous) clones. Maximum-parsimony and maximum-likelihood analyses of mitochondrial DNA sequence data from specimens collected across Western Europe showed that asexuality, which does not appear to be caused by the bacterium Wolbachia, is concentrated in two geographically widespread lineages, the older of which diverged from the closest extant sexual taxa approximately 0.5 million years ago. However, the DNA sequences of a nuclear intron (elongation factor—1α) showed no congruence with this pattern, and a much higher frequency of heterozygotes with very high allelic diversity was observed among the asexual females compared to that among females from the sexual species. This pattern is consistent with maternally inherited asexuality coupled with a history of rare sex with members of several closely related sexual populations or species. Our observations reinforce recent arguments that rare sex may be more important for the persistence of otherwise asexual lineages than hitherto appreciated.     

Habitat assessment by parasitoids: consequences for population distribution

The ideal free distribution (IFD) is a stable distribution ofcompetitors among resource patches. For equally efficient competitors,equilibrium is reached when the per capita rate of intake equalizesacross patches. The seminal version of the IFD assumes omniscience,but populations may still converge toward the equilibrium providedthat competitors 1) accurately assess their environment by learningand 2) remain for an optimal (rate-maximizing) time on eachencountered patch. In the companion article (Tentelier C, DesouhantE, Fauvergue X. 2006. Habitat assessment by parasitoids: mechanismsfor patch time allocation. Behav Ecol. Forthcoming), it is shownthat the parasitoid wasp Lysiphlebus testaceipes adapts itsexploitation of aphid host colonies based on previous experience,in a manner consistent with these two conditions. We thereforepredicted that a randomly distributed population of initiallynaive wasps should converge toward the IFD. We tested this predictionby introducing 1300 L. testaceipes females into a 110-m² greenhousecontaining 40 host patches. Just after introduction, the parasitoidrate of gain was positively affected by host number and negativelyaffected by parasitoid number but, as predicted, these effectsvanished in the course of the experiment. Six hours after introduction,the expected rate of gain reached a constant. Surprisingly,this passage through equilibrium was not accompanied by a decreasein the coefficient of variation among gain rates or by a shiftfrom a random to an aggregated distribution of parasitoids.These results challenge our understanding of the link betweenindividual behavior and population distribution.     

茶足柄瘤蚜茧蜂对苜蓿蚜的寄生功能反应

在室内(25±1℃,L:D=16:8光周期,RH=40%～60%)条件下,研究了茶足柄瘤蚜茧蜂Lysiphlebus testaceipes(Cresson)对苜蓿蚜Aphis craccivora(Koch)若蚜的寄生功能反应。结果表明:苜蓿蚜的龄期对茶足柄瘤蚜茧蜂的寄生作用有很大影响,用功能反应HollingⅡ模型模拟,其模拟方程为Na=1.118 N/(1+0.0184 N)。通过该方程可明确单头雌成蜂在24 h内最多寄生60.60头苜蓿蚜,其寄生1头苜蓿蚜所需时间为0.396 h。在5个温度梯度下,茶足柄瘤蚜茧蜂对苜蓿蚜的寄生功能反应均符合HollingⅡ模型,但不同温度下的功能反应参数有明显的差异。此外茶足柄瘤蚜茧蜂自身密度对寄生有一定的干扰作用,其干扰作用通过Hassell-Varley模型拟合,方程为a=0.0621P-0.3062,表明茶足柄瘤蚜茧蜂雌蜂的发现域随着自身密度的增加而逐渐变小,寄生蜂雌蜂个体间的相互干扰效应降低了寄生效能。     

Parasitoids use herbivore-induced information to adapt patch exploitation behaviour

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

Foraging patterns of two aphid parasitoids, Lysiphlebus testaceipes and Aphidius colemani on banana

The searching behaviour of two aphid parasitoids, Lysiphlebus testaceipes (Cresson) and Aphidius colemani Viereck (Hymenoptera, Aphidiidae), was analysed. Both species searched banana plants (Musa spec.) infested with the banana aphid Pentalonia nigronervosa Coq. in a different way. L. testaceipes restricted its search to open plant structures and avoided concealed areas. A. colemani partitioned its time spent on the plant between open and concealed areas. This general pattern was independent of aphid colony size and was also observed in the absence of aphids. As a consequence of these searching tactics, the borders of a host patch differed for both parasitoid species. For L. testaceipes, the patch consisted only of aphids feeding on open structures, while it comprised the whole aphid colony for A. colemani. The observed searching patterns resulted in a different exploitation of the aphid colonies.

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Zusammenfassung Eine Analyse des Suchverhaltens der beiden Blattlausparasitoide Lysiphlebus testaceipes (Cresson) and Aphidius colemani Viereck zeigte, daß beide Arten Bananenpflanzen (Musa spec.), die von der Bananenblattlaus Pentalonia nigronervosa Coq. befallen waren, auf unterschiedliche Weise absuchten. L. testaceipes beschränkte seine Wirtssuche auf frei zugängliche Pflanzenteile und vermied ein Eindringen in geschützte Pflanzenstruckturen. Dagegen hielt sich A. colemani gleichermaßen häufig auf offenen und in geschützten Pflanzenteilen auf. Dieses generelle Suchmuster war unabängig von der Blattlauskoloniegröß und wurde auch beim Fehlen von Wirten beobachtet. Als Konsequenz aus diesem unterschiedlichen Suchverhalten ergaben sich verschiedene Patchgrenzen für beide Parasitoide. Für L. testaceipes bestand der Patch nur aus Blattläusen, die an frei zugänglichen Pflanzenstrukturen saugten, während der Patch für A. colemani alle Blattläuse einschließlich der Tiere umfaßte, die sich in geschützten Pflanzenteilen aufhielten. Damit führte dieses unterschiedliche Suchverhalten beider Parasitoidenarten zu einer unterschiedlichen Ausnutzung der Blattlauskolonien.