Temperature influences the handling efficiency of an aphid parasitoid through body size-mediated effects

It is well known that increasing the ambient temperature increases the metabolic rate and consequently, the foraging rate of most insects. However, temperature experienced during the immature stages of insects affects their adult size (an inverse relationship). Because body size is generally correlated to foraging success, we hypothesized that temperature indirectly influences the foraging efficiency of adult insects through developmental effects. We first investigated the role of parasitoid: host body size ratio on the handling time of Aphidius colemani (Viereck) (Hymenoptera: Braconidae), then tested the prediction that increasing temperature during immature development increases the handling time of adults. As expected, parasitoids took longer to handle large aphids than small aphids. However, large parasitoids did not have shorter handling times than small parasitoids except when attacking large (adult) aphids. Developmental temperature had the predicted effect on parasitoids: Individuals reared at 25°C were smaller than those insects reared at 15°C. Parasitoids reared at 15°C had similar short handling times for both first instar and adult aphids, whereas parasitoids reared at 25°C took longer to handle adult aphids than first instar aphids. The size-mediated effect of temperature through development on parasitoid efficiency was opposite to the more familiar direct effect of temperature through metabolic rate. We conclude that the net effect of temperature on foraging insects will depend on its relative influence on immature and adult stages.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

Life history ofAphis gossypii on cucumber: influence of temperature, host plant and parasitism

Life table data forAphis gossypii Glover (Homoptera: Aphididae), an important pest in glasshouse cucumber crops, were studied at 20, 25 and 30°C on two cucumber cultivars (Cucumis sativus L.) in controlled climate cabinets. The development time on the cucumber cv. ‘Sporu’ ranged from 4.8 days at 20°C to 3.2 days at 30°C. Immature mortality was approximately 20% and did not differ between temperatures. Most mortality occurred during the first instar. Reproduction periods did not differ among temperatures, but at 25 and 30°C more nymphs were produced (65.9 and 69.8 nymphs/♀, respectively) than at 20°C (59,9 nymphs/♀) because of a higher daily reproduction. Intrinsic rate of increase was greatest at 25°C (r _m =0.556 day⁻¹). At 20 and 30°C the intrinsic rate of increase was 0.426 and 0.510, respectively. On cv. ‘Aramon’, the development time ofA. gossypii was approximately 20% longer at all temperatures. Immature mortality did not differ between the two cultivars. The intrinsic rate of increase on cv. ‘Aramon’ was 15% smaller than on cv. ‘Sporu’. The use of cucumber cultivars partially resistant to aphids is discussed in relation to biological control of cotton aphid in glasshouses. Development time and immature mortality on leaves of the middle and upper leaf layer of glasshouse grown cucumber plants (cv. ‘Aramon’) were comparable to development in the controlled climate cabinets. On the lower leaves immature mortality was much higher (approximately 82%) than on leaves of the middle (24.0%) and upper leaf layer (24.5%). Reproduction was less on the lower leaf layer (45.9, 70.5 and 70.1 nymphs/♀ on leaves of the lower, middle and upper leaf layer, respectively). Aphids, successfully parasitized byAphidius colemani Viereck (Hymenoptera: Braconidae) only reproduced when they were parasitized after the third instar. Fecundity was 0.1 to 0.9 and 10.5 to 13.3 nymphs/♀ for aphids parasitized in the fourth instar or as adults, respectively. Reproduction of aphids that were stung but survived the attack was lower than for aphids not stung. Average longevity of these aphids was equal to the longevity of aphids not stung byA. colemani.     

Host Age Preference Behavior in <Emphasis Type="Italic">Aphidius ervi</Emphasis> Haliday (Hymenoptera: Aphidiidae)

Many parasitoid species have preference for certain stages of hosts to parasitize but the underlying behavioral mechanisms of such preference are still poorly understood, making it difficult to evaluate host-parasitoid interactions and their effects on the success of biological control programs. Here, we report our work on a parasitoid Aphidius ervi Haliday on the pea aphid Acyrthosiphon pisum (Harris). We show that with the increase of host age, female parasitoids are more likely to encounter and to attack their hosts but the hosts develop increasingly greater defensive capabilities. Encounter almost always triggers attack attempt; however, increasing attack attempts do not proportionally lead to ovipositor probings and increasing ovipositor probings do not proportionally translate into ovipositions. These asymmetric responses may be interpreted as that A. ervi females prefer to parasitize older aphids for higher fitness return but those aphids can better defend themselves, and as a consequence, A. ervi females may achieve the highest gain by attacking aphids of intermediate ages. We suggest that A. ervi females forage in a manner consistent with the optimal foraging theory, trading off host handling time with fitness returns.     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.     

Host stage selection of the mealybug parasitoid Anagyrus spec. nov near sinope

The mealybug parasitoid Anagyrus spec. nov near sinope (Hymenoptera: Encyrtidae) is an undescribed parasitoid of the Madeira mealybug, Phenacoccus madeirensis Green (Homoptera: Pseudococcidae). We investigated the preference of Anagyrus spec. nov near sinope for six developmental stadia (first‐ and second‐instar nymphs, third‐instar immature females, third‐ or fourth‐instar immature males, pre‐reproductive adult females, and ovipositing adult females) of P. madeirensis and the fitness consequences of the host stage selection behavior. In the no‐choice test, Anagyrus spec. nov near sinope parasitized and completed development in all host stadia except third‐instar immature males. When all host stadia were offered simultaneously, the parasitoids preferred third‐instar immature and pre‐reproductive adult females. Dissection of the stung mealybugs revealed that the clutch size (number of eggs per host) was approximately four and three in the third‐instar and pre‐reproductive females, respectively, and one egg per first‐instar nymph. Parasitoids emerged from P. madeirensis parasitized at third‐instar or pre‐reproductive adult female completed development in the shortest duration, achieved a higher progeny survival rate, larger brood and body size, and the lowest proportion of males. We showed that the continued development of mealybugs had significant influence on the fitness of the parasitoids. Although deposited as eggs in first‐ or second‐instar nymphs, parasitoids emerged from mummies that had attained third‐instar or adult development achieved similar progeny survival rate, brood size, body size, and sex ratio as those parasitoids deposited and developed in third‐instar or adult mealybugs. By delaying larval development in young mealybugs, Anagyrus spec. nov near sinope achieved higher fitness by allowing the parasitized mealybugs to grow and accumulate body size and resources. We suggest that the fitness consequence of host stage selection of a koinobiont parasitoid should be evaluated on both the time of parasitism and the time of mummification.     

Performance of the parasitoid Aphidius colemani when reared on Myzus persicae on a fully defined artifical diet

Aphidius colemani Viereck(Hymenoptera: Aphidiidae) showed a developmenttime extended by 16% when reared on Myzus persicae Sulzer (Hemiptera: Aphididae) ofdifferent instars on artificial diet or onaphids on Brussels sprout plants. There wasalso a small but statistically significant 2%reduction in size (in hind tibia length) ofadult females. Rearing on diet had nosignificant effect on the number of eggsfemales contained at emergence. In a secondexperiment, aphids from Brussels sprouts ininstars 2–5 were compared with aphids from diettwo days older to give comparably sized aphidsfrom both substrates. Parasitisation by A.colemani gave the same direction of results,but showed that the effects in the firstexperiment were greater than predicted from thereduction in host size alone. However, in bothexperiments effects on parasitoids ofdiet-rearing the host were small, and culturingA. colemani on diet-reared aphids wassuccessful.     

Influence of aphid size,age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models

Summary When host quality varies, parasitoid wasps are expected to oviposit selectively in high-quality hosts. We tested the assumption underlying host-size models that, for solitary species of wasps, quality is based on host size. Using Ephedrus californicus, a solitary endoparasitoid of the pea aphid, we evaluated the influence of aphid size (= mass), age and defensive behaviours on host selection. Experienced parasitoid females were given a choice among three classes of 5-day-old apterous nymphs: small aphids that had been starved daily for 4 h (S4) and 6 h (S6) respectively, and large aphids permitted to feed (F) normally. Wasps attacked more, and laid more eggs in, small than large aphids (S6>S4>F). This rank-order for attack did not change when females could choose among aphids of the same size that differed in age; however, wasps oviposited in all attacked aphids with equal probability. Host size did not influence parasitoid attack rates when aphids were anaesthetized so that they could not escape or defend themselves. As predicted by host-size models, wasp size increased with host size (F>S4; S6), but large wasps required longer to complete development than their smaller counterparts (S4E. californicus reflects a trade-off between maximization of fitness gains per egg and the economics of search-time allocation. Because large aphids are more likely to escape parasitization, a wasp must balance her potential gain in fitness by ovipositinng in a high-quality (large) aphid against her potential cost in terms of lost opportunity time if the attack fails.     

Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plant–herbivore system. First, the olfactory response of females was tested in a Y‐tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or plant–host complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore‐induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant.     

All Clone-mates are not Created Equal: Fitness Discounting Theory Predicts Pea Aphid Colony Structure

As many animals form aggregations, group-living is believed to be adaptive. It is not clear, though, if clonal aggregations should have spatial structure, as protecting clone-mates is the genetic equivalent of protecting self. ‘Fitness discounting’ theory states that immediate reproductive opportunities are of greater value than are delayed opportunities. Thus, we hypothesized that spatial structure should exist in colonies of unequal-aged, clonal organisms like aphids. We predicted that, compared to reproductive (5^th instar) individuals, young (2^nd and 3^rd instar) juveniles (i.e., the youngest instars capable of emitting an alarm signal) should occupy the most dangerous feeding positions. As individuals approach reproductive maturity and alarm signals decline (4^th instar), they should occupy increasingly safer feeding positions. We tested these predictions by documenting the spatial distribution of two (green and pink) pea aphid, Acyrthosiphon pisum, asexual lineages (“clones”) at 1, 3, 6, 24, 48, 72, 96, and 120 h after host plant colonization. Confirming our hypothesis, we found that early (2^nd and 3^rd) instar aphids occupied feeding positions with the highest predation risk. Upon reaching the penultimate (4^th) instar, individuals dispersed from the colony to colonize other leaves. Thus, pea aphid colonies are not random aggregations; aphid colony structure can be explained by fitness discounting theory.     

Host plant genotype determines bottom‐up effects in an aphid‐parasitoid‐predator system

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species

We measured the acceptance and suitability of four aphid species [Aphis gossypii Glover, Myzus persicae (Sulzer), Rhopalosiphum padi (L.), and Schizaphis graminum (Rondani)] (Homoptera: Aphididae) for the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Female parasitoids parasitized fewer R. padi than the other three aphid species, and fewer offspring successfully completed development in R. padi than in the other three host species. Sex ratios of emerging adults were more male‐biased from R. padi than from the other three aphid species, suggesting that R. padi is a poor quality host for this population of A. colemani. Ovipositing A. colemani encountered R. padi at a slower rate, spent more time handling R. padi, and parasitoid offspring died at a higher rate in R. padi compared to A. gossypii. Our results show that oviposition behavior and offspring performance are correlated. In each experiment, we tested the effect of the host species in which the parasitoids developed (parental host) on the number of hosts attacked, the proportion of each host species accepted for oviposition and the survival of progeny. Parental host affected maternal body size and, through its effect on body size, the rate of encounter with hosts. Other than this, parental host species did not affect parasitism.     

The influence of temperature on size as an indicator of host quality for the development of a solitary koinobiont parasitoid

The influence of aphid size on the host quality assessment and progeny performance of aphidiine parasitoids was examined using the mealy plum aphid parasitoid, Aphidius transcaspicus Telenga (Hymenoptera: Braconidae) and the black bean aphid, Aphis fabae Scopoli (Homoptera: Aphididae), as a readily acceptable alternate host. Aphid size in relation to stage of development was manipulated by rearing synchronous aphid cohorts at either 15 or 30 °C. At 15 °C, 2nd instar aphids were approximately the same size as 4th instar aphids reared at 30 °C. Cohorts of 30 aphids from each instar, reared at each temperature, were exposed to parasitism by a single parasitoid female for a period of 5 h. Overall susceptibility to parasitism did not vary between aphid cohorts, but the parasitoid response to aphid size differed significantly between rearing temperatures for both progeny sex ratio (parent female assessment of host quality) and larval growth and development (host suitability for parasitoid development). For aphids reared at 15 °C, the proportion of female progeny and emerging adult size for the parasitoid increased linearly with aphid size at the time of attack, while development time remained constant. In contrast, for aphids reared at 30 °C, the proportion of female progeny, emerging adult size, and the development time of the parasitoid all declined with aphid size at the time of attack. The contrasting responses of the parasitoid to host size for aphids reared at the two temperatures suggest that host quality is only indirectly related to aphid size among aphidiine parasitoids. The possible effects of higher temperatures on nutritional stress, obligate endosymbionts, and future growth potential of the aphids are discussed as explanations for the variation in host quality for parasitoid development.     

Population expansion in the North African Late Pleistocene signalled by mitochondrial DNA haplogroup U6

Background

Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. Altruistic behaviours can evolve through indirect fitness benefits when directed toward kin. The altruistic nature of anti-predatory behaviours is often difficult to establish because the actor can obtain direct fitness benefits, or the behaviour could result from selfish coercion by others, especially in eusocial animals. Non-eusocial parthenogenetically reproducing aphids form colonies of clone-mates, which are ideal to test the altruistic nature of anti-predatory defence behaviours. Many aphids release cornicle secretions when attacked by natural enemies such as parasitoids. These secretions contain an alarm pheromone that alerts neighbours (clone-mates) of danger, thereby providing indirect fitness benefits to the actor. However, contact with cornicle secretions also hampers an attacker and could provide direct fitness to the actor.

Results

We tested the hypothesis that cornicle secretions are altruistic by assessing direct and indirect fitness consequences of smearing cornicle secretions onto an attacker, and by manipulating the number of clone-mates that could benefit from the behaviour. We observed parasitoids, Aphidius rhopalosiphi, foraging singly in patches of the cereal aphid Sitobion avenae of varied patch size (2, 6, and 12 aphids). Aphids that smeared parasitoids did not benefit from a reduced probability of parasitism, or increase the parasitoids' handling time. Smeared parasitoids, however, spent proportionately more time grooming and less time foraging, which resulted in a decreased host-encounter and oviposition rate within the host patch. In addition, individual smearing rate increased with the number of clone-mates in the colony.

Conclusions

Cornicle secretions of aphids were altruistic against parasitoids, as they provided no direct fitness benefits to secretion-releasing individuals, only indirect fitness benefits through neighbouring clone-mates. Moreover, the use of cornicle secretions was consistent with their altruistic nature, because the occurrence of this behaviour increased with the size of indirect fitness benefits, the number of clone-mates that can benefit. This study provides evidence for a case of kin-directed altruistic defence outside eusocial animals.     

Influence of cornicle droplet secretions of the cabbage aphid,Brevicoryne brassicae,on parasitism behavior of na＇fve and experienced Diaeretiella rapae

Insects have evolved amazing methods of defense to ward off enemies. Many aphids release cornicle secretions when attacked by predators and parasitoids. These se cretions contain an alarm pheromone that alerts other colony members of danger, thereby providing indirect fitness benefits to the releaser. In addition, contact with cornicle se cretions could also threaten an attacker and could provide direct fitness to the releaser. However, cornicle secretions may also be recruited as a kairomonal cue by aphid natural enemies. In this study, we investigated the effect of the cornicle droplet volatiles of the cabbage aphid, Brevicoryne brassicae （L.）, on the hostsearching behavior of naive and experienced female Diaeretiella rapae （M＇Intosh） parasitoids in olfactometer studies. In addition, we evaluated the role ofB. brassicae cornicle droplets on the oviposition prefer ence of the parasitoid in a twochoice bioassay. Naive females did not exhibit any preference between volatiles from aphids secreting cornicle droplets over nonsecreting aphids, while experienced parasitoids exploited the secretions in their host location. Experienced females were also able to choose volatiles from both secreting and nonsecreting aphids over clean air, while this ability was not observed in naive females. Although secretion of cornicle droplets did not influence the percentage of first attack in either naive or experienced females, the success of attack （i.e. resulting in a larva） was significantly different between secreting and nonsecreting aphids in the case of experienced parasitoids.     

The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size

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Larvicidal activity of lectins onLucilia cuprina: mechanism of action

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