Leaf surface wax and plant morphology of peas influence insect density

Insect predators and parasitoids adhere better, forage more effectively, and take more aphid prey on pea plants (Pisum sativum L.) (Leguminosae) with mutations that reduce the crystalline wax bloom on the plant surface. To assess the agronomic potential of this trait for pest management, abundance of pea aphids (Acyrthosiphon pisum L.) (Homoptera: Aphididae) and coccinellid predators, and percent parasitism of the aphids were evaluated on pea lines differing in wax bloom and plant architecture over two field seasons. Three pairs of pea lines were evaluated, each pair with a different architecture and differing within the pair in the amount of surface wax bloom (reduced or normal). The trials included plots treated with a narrow spectrum insecticide (pymetrozine) to reduce aphid populations and untreated controls. Reduced wax peas had significantly fewer aphids per plant in 2002 but not in 2003. Total natural enemy abundance was greater on reduced wax than on normal wax pea lines in both years of the study. Pymetrozine reduced aphid densities significantly in both years. Among the four pea lines evaluated for yield, seed yield per plant was affected by plant morphology and insecticide treatment. Yield was greatest on semileafless plants and on pymetrozine sprayed plots in both years. Yield of the reduced wax line in the semileafless background was similar to or exceeded yield in its normal wax sister line, suggesting that this morphological type was best for an agronomically viable reduced wax phenotype. Pea weevil (Bruchus pisorum L.) (Coleoptera: Bruchidae) damage to seed was overall more frequent on seeds from reduced wax varieties than from normal wax varieties. The results illustrate the trade‐offs associated with a reduced wax trait in peas but also show that certain combinations of reduced wax and gross morphology lead to reduced pea aphid populations and yields similar to those of normal wax peas.     

Delineating the effects of a plant trait on interactions among associated insects

Plant traits can affect ecological interactions between plants, herbivores, and predators. Our study tests whether reduced leaf wax in peas alters the interaction between the pea aphid ( Acyrthosiphon pisum), a foliar-foraging predator (a lady beetle, Hippodamia convergens) and a ground-foraging predator (a ground beetle, Poecilus scitulus). We performed a 2×2×2 factorial experiment in which wax level, presence of H. convergens, and presence of P. scitulus were manipulated. Experimental arenas consisted of a cage surrounding three pea plants. One plant in each cage was stocked with 15 pea aphids. In greenhouse and field cage experiments, we assessed the effect of each factor and their interactions on aphid density. As in previous studies, H. convergens foraged for aphids more effectively on reduced wax peas than on normal peas. Other interactions among H. convergens, P. scitulus , and A. pisum were the same on both types of peas. We consider how aphid movement, plant growth, and a high frequency of predation by P. scitulus on H. convergens influenced pea aphid density.     

A plant surface mutation mediates predator interference among ladybird larvae

Abstract.  1. We investigated mechanisms causing predator–predator interference between fourth instar Hippodamia convergens larvae foraging for pea aphids on pea plants, Pisum sativum , with a wild-type wax bloom, and the lack of such interference between larvae foraging on pea plants with a reduced-wax bloom caused by the single gene mutation wel .
2. Observations showed that behavioural interactions between larvae were not affected by wax phenotype. Specifically, larvae did not encounter one another more frequently on normal-wax peas as may have been predicted because reduced ability by coccinellids to attach to normal-wax plant surfaces could restrict them to foraging on only some parts of these plants.
3. In a controlled bioassay on normal-wax peas, H. convergens larvae avoided leaflets previously exposed to another larva. On reduced-wax peas, this effect was not detected.
4. In microcosm experiments, inter-predator interference in terms of prey consumption occurred on normal-wax peas, but not on reduced-wax peas. The interference on normal-wax peas occurred whether two H. convergens larvae were placed on a pea aphid-infested, normal-wax plant simultaneously or sequentially.
5. We conclude that the observed inter-predator interference is not as a result of direct physical contact, but rather arises because of (i) inhibition of foraging by chemical trails left by other larvae, (ii) the inability of larvae to access portions of the normal-wax plants creating aphid refugia, or (iii) a combination of these factors.     

Aphid population dynamics: does resistance to parasitism influence population size?

1. Insect population size is regulated by both intrinsic traits of organisms and extrinsic factors. The impacts of natural enemies are typically considered to be extrinsic factors, however insects have traits that affect their vulnerability to attack by natural enemies, and thus intrinsic and extrinsic factors can interact in their effects on population size. 2. Pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in New York and Maryland that are specialised on alfalfa are approximately two times more physiologically resistant to parasitism by Aphidius ervi Haliday (Hymenoptera: Braconidae) than pea aphids specialised on clover. To assess the potential influence of this genetically based difference in resistance to parasitism on pea aphid population dynamics, pea aphids, A. ervi, and other natural enemies of aphids in clover and alfalfa fields were sampled. 3. Rates of successful parasitism by A. ervi were higher and pea aphid population sizes were lower in clover, where the aphids are less resistant to parasitism. In contrast, mortality due to a fungal pathogen of pea aphids was higher in alfalfa. Generalist aphid predators did not differ significantly in density between the crops. 4. To explore whether intrinsic resistance to parasitism influences field dynamics, the relationship between resistance and successful field parasitism in 12 populations was analysed. The average level of resistance of a population strongly predicts rates of successful parasitism in the field. The ability of the parasitoid to regulate the aphid may vary among pea aphid populations of different levels of resistance.     

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.     

Impact of environmental stress on aphid clonal resistance to parasitoids: Role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid

Resistance to endoparasitoids in aphids involves complex interactions between insect and microbial players. It is now generally accepted that the facultative bacterial symbiont Hamiltonella defensa of the pea aphid Acyrthosiphon pisum is implicated in its resistance to the parasitoid Aphidius ervi. It has also been shown that heat negatively affects pea aphid resistance, suggesting the thermosensitivity of its defensive symbiosis. Here we examined the effects of heat and UV-B on the resistance of A. pisum to A. ervi and we relate its stability under heat stress to different facultative bacterial symbionts hosted by the aphid. For six A. pisum clones harboring four different facultative symbiont associations, the impact of heat and UV-B was measured on their ability to resist A. ervi parasitism under controlled conditions. The results revealed that temperature strongly affected resistance, while UV-B did not. As previously shown, highly resistant A. pisum clones singly infected with H. defensa became more susceptible to parasitism after exposure to heat. Interestingly, clones that were superinfected with H. defensa in association with a newly discovered facultative symbiont, referred to as PAXS (pea aphid X-type symbiont), not only remained highly resistant under heat stress, but also expressed previously unknown, very precocious resistance to A. ervi compared to clones with H. defensa alone. The prevalence of dual symbiosis involving PAXS and H. defensa in local aphid populations suggests its importance in protecting aphid immunity to parasitoids under abiotic stress.     

Plant waxy bloom on peas affects infection of pea aphids by Pandora neoaphidis

This study examined the effects of the surface wax bloom of pea plants, Pisum sativum, on infection of pea aphids, Acyrthosiphon pisum, by the fungal pathogen Pandora neoaphidis. In prior field surveys, a higher proportion of P. neoaphidis-killed pea aphids (cadavers) had been observed on a pea line with reduced wax bloom, as compared with a sister line with normal surface wax bloom. Laboratory bioassays were conducted in order to examine the mechanisms. After plants of each line infested with aphids were exposed to similar densities of conidia, the rate of accumulation of cadavers on the reduced wax line was significantly greater than on the normal wax bloom line; at the end of the experiment (13d), the proportion of aphid cadavers on the reduced wax line was approximately four times that on the normal wax bloom line. When plants were exposed to conidia first and then infested with aphids, the rate of accumulation of cadavers was slightly but significantly greater on the reduced wax line, and infection at the end of the experiment (16d) did not differ between the lines. When aphids were exposed first and then released onto the plants, no differences in the proportion of aphid cadavers were observed between the pea lines. Greater infection of pea aphid on reduced wax peas appears to depend upon plants being exposed to inoculum while aphids are settled in typical feeding positions on the plant. Additional experiments demonstrated increased adhesion and germination by P. neoaphidis conidia to leaf surfaces of the reduced wax line as compared with normal wax line, and this could help explain the higher infection rate by P. neoaphidis on the reduced wax line. In bioassays using surface waxes extracted from the two lines, there was no effect of wax source on germination of P. neoaphidis conidia.     

The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct?

Predation or parasitism on species introduced as biological control agents is a common explanation for failure of biological control programs. Although there is clear evidence from some biological control programs that hyperparasitism can impact a parasitoid biological control agent, it is not clear whether hyperparasitoids have the potential to cause control failure. We performed glasshouse experiments using cages containing 48 plants to address whether the hyperparasitoid Asaphes suspensus can potentially eliminate a population of the primary parasitoid Aphidius ervi, a biological control agent of the pea aphid Acyrthosiphon pisum. Although As. suspensus has a low intrinsic rate of increase, only one-half that of A. ervi and one-third that of pea aphids, it was nonetheless capable of eliminating the A. ervi population within seven A. ervi generations. In contrast, in the absence of As. suspensus, A. ervi eliminated the pea aphid population. Field surveys, however, found that As. suspensus does not eliminate entire natural populations of A. ervi in lucerne crops, probably due to the high frequency of disturbance that favours high intrinsic rates of increase and short generation times. Nonetheless, the ability of As. suspensus to eliminate A. ervi in cages despite its low intrinsic rate of increase underscores the potential for hyperparasitism to disrupt biological control. Small populations are expected to be particularly susceptible to hyperparasitism, such as when releases of a new biological control agent are made.     

Patterns of host selection by four species of aphidiid (Hymenoptera) parasitoids: influence of host switching

Abstract.

• 1 We tested switching behaviour in four species of aphidiid parasitoids, using a two-aphid experimental system consisting of second-instar nymphs of pea aphid (Acyrthosiphon pisum (Harris)) and alfalfa aphid (Macrosiphum creelii Davis) feeding on broad beans in the laboratory.
• 2 Aphidius ervi Haliday, A.pisivorus Smith, A.smithi Sharma & Subba Rao, and Pram pequodorum Viereck showed an innate preference for pea aphid when both host species were provided in equal numbers.
• 3 Wasps encountered both aphid species equally but differed in their acceptance of alfalfa aphid. Females of A.pisivorus and P.pequodorum accepted alfalfa aphids when few pea aphids were available, but A. smithi always concentrated attacks on pea aphid. Aphidius ervi super-parasitized an increasing proportion of pea aphids as their availability declined.
• 4 Switching to the alfalfa aphid occurred in A.ervi and P.pequodorum (but not in A.pisivorus and A.smithi) under the condition of a 1:3 ratio of pea aphids:alfalfa aphids. Wasps did not switch when more pea aphids than alfalfa aphids were provided (3:1 ratio).
• 5 Alfalfa aphids were more likely than pea aphids to escape from parasitoid attack.
• 6 Switching to the most abundant host may not be adaptive in these four species of aphid parasitoids. A foraging wasp incurs a potentially higher cost in lost opportunity time when attacking (and failing to oviposit in) alfalfa aphids. In addition, alfalfa aphids may have lower host quality than pea aphids, a difference that could influence offspring fitness.

     

EVOLUTION OF AN APHID-PARASITOID INTERACTION: VARIATION IN RESISTANCE TO PARASITISM AMONG APHID POPULATIONS SPECIALIZED ON DIFFERENT PLANTS

The evolution of associations between herbivorous insects and their parasitoids is likely to be influenced by the relationship between the herbivore and its host plants. If populations of specialized herbivorous insects are structured by their host plants such that populations on different hosts are genetically differentiated, then the traits affecting insect-parasitoid interactions may exhibit an associated structure. The pea aphid (Acyrthosiphon pisum) is a herbivorous insect species comprised of genetically distinct groups that are specialized on different host plants (Via 1991a, 1994). Here, we examine how the genetic differentiation of pea aphid populations on different host plants affects their interaction with a parasitoid wasp, Aphidius ervi. We performed four experiments. (1) By exposing pea aphids from both alfalfa and clover to parasitoids from both crops, we demonstrate that pea aphid populations that are specialized on alfalfa are successfully parasitized less often than are populations specialized on clover. This difference in parasitism rate does not depend upon whether the wasps were collected from alfalfa or clover fields. (2) When we controlled for potential differences in aphid and parasitoid behavior between the two host plants and ensured that aphids were attacked, we found that pea aphids from alfalfa were still parasitized less often than pea aphids from clover. Thus, the difference in parasitism rates is not due to behavior of either aphids or wasps, but appears to be a physiologically based difference in resistance to parasitism. (3) Replicates of pea aphid clones reared on their own host plant and on a common host plant, fava bean, exhibited the same pattern of resistance as above. Thus, there do not appear to be nutritional or secondary chemical effects on the level of physiological resistance in the aphids due to feeding on clover or alfalfa, and therefore the difference in resistance on the two crops appears to be genetically based. (4) We assayed for genetic variation in resistance among individual pea aphid clones collected from clover fields and found no detectable genetic variation for resistance to parasitism within two populations sampled from clover. This is in contrast to Henter and Via's (1995) report of abundant genetic variation in resistance to this parasitoid within a pea aphid population on alfalfa. Low levels of genetic variation may be one factor that constrains the evolution of resistance to parasitism in the populations of pea aphids from clover, leading them to remain more susceptible than populations of the same species from alfalfa.     

<Emphasis Type="Italic">Aphidius ervi</Emphasis> Preferentially Attacks the Green Morph of the Pea Aphid, <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis>

The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae) is found in red and green color morphs. Previous work has suggested that the aphidiine parasitoid Aphidius ervi Haliday preferentially attacks green pea aphids in the field. It is not clear whether these results reflect a real preference, or some unknown clonal difference, such as in immunity, between the aphids used in the previous studies. We used three susceptibility-matched pairs of red and green morph pea aphid clones to test for preferences. In a no-choice situation, the parasitoids attacked equal proportions of each color morph. When provided with a choice, A. ervi was significantly more likely to oviposit into colonies formed from green morphs when the neighboring colony was formed from red morph aphids. In contrast, red morphs were less likely to be attacked when their neighboring colony was of the green morph. By preferentially attacking green colonies, A. ervi may reduce the likelihood of intraguild predation, as it is suggested that visually foraging predators preferentially attack red aphid colonies. Furthermore, if this host choice behavior is replicated in the field, we speculate that color morphs of the pea aphid may interact indirectly through their shared natural enemies, leading to intraspecific apparent competition.     

Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance

Interactions between natural enemies can be crucial for determining their overall control of pest species, yet the mechanisms that govern such interactions are often poorly understood. The risk of negative effects such as intraguild predation and the possibility of mitigating such risks are important components for ultimately determining the compatibility of biological control agents. We performed a group of experiments to determine whether the coccinellid Harmonia axyridis Pallas (Coleoptera: Coccinellidae) poses an intraguild threat to the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) and to see whether A. ervi is able to avoid predation by responding to the chemical tracks deposited by H. axyridis. We show that although H. axyridis does not readily consume A. ervi mummies, it preferentially consumes parasitized aphids over unparasitized aphids. We also show that A. ervi can defend against this threat by avoiding oviposition in the presence of H. axyridis chemical tracks. Aphidius ervi parasitized far fewer pea aphids Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) on plants [Vicia faba L. (Fabaceae)] with H. axyridis chemical tracks in a no‐choice environment at a single‐plant scale. Similarly, when parasitoids could move freely between plants with and without tracks, A. ervi parasitism was higher on plants without tracks. Behavioral observations of A. ervi foraging suggested that this might be because of reduced A. ervi attack rates and patch residence times in the presence of H. axyridis tracks. Despite a risk of intraguild predation by H. axyridis, our study suggests that A. ervi may be able to mitigate this risk by altering its behavior in response to chemical cues.     

Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector

• 1 Aphids are the major group of insects that vector plant viruses, and they often display a preference for foliage showing disease symptoms. Although this behaviour will increase the numbers of vectors acquiring the pathogen, it will not in itself result in a greater spread of the disease.
• 2 The present study examined how infection of Vicia faba by the nonpersistently transmitted virus bean yellow mosaic virus (BYMV) affected colonization by pea aphids Acyrthosiphon pisum. We then examined how foraging by the hymenopterous parasitoid Aphidius ervi affected aphid settling/movement behaviour and the consequences for dissemination of the virus.
• 3 In Petri dish arenas, aphids colonized discs from BYMV‐infected leaves more rapidly than discs from uninfected plants. Reflectance from infected foliage was approximately 20% higher than from uninfected leaves in the green–yellow wavelengths, indicating that aphids might be responding to visual cues from the brighter foliage. Settling was reduced by A. ervi, with the foraging wasps preventing the aphids reaching and/or remaining on the leaf tissue.
• 4 In multiple plant arenas, A. ervi caused a reduction in aphid numbers but also a nine‐fold increase in BYMV infection. It is hypothesized that disturbance by the parasitoids resulted in more aphid movement as well as more cases of aphids probing on a BYMV‐infected plant and then a new host within the critical time period for successful inoculation to occur. This effect of parasitoids on virus dispersal should be considered in epidemiological models of insect‐vectored plant diseases, and also when evaluating the use of natural enemies in biocontrol strategies of insect herbivore/vector pests.

     

Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Insects harbour a wild diversity of symbionts that can spread and persist within populations by providing benefits to their host. The pea aphid Acyrthosiphon pisum maintains a facultative symbiosis with the bacterium Hamiltonella defensa, which provides enhanced resistance against the aphid parasitoid Aphidius ervi. Although the mechanisms associated with this symbiotic‐mediated protection have been investigated thoroughly, little is known about its evolutionary effects on parasitoid populations. We used an experimental evolution procedure in which parasitoids were exposed either to highly resistant aphids harbouring the symbiont or to low innate resistant hosts free of H. defensa. Parasitoids exposed to H. defensa gained virulence over time, reaching the same parasitism rate as those exposed to low aphid innate resistance only. A fitness reduction was associated with this adaptation as the size of parasitoids exposed to H. defensa decreased through generations. This study highlighted the considerable role of symbionts in host–parasite co‐evolutionary dynamics.     

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.     

Effect of Adult Experience on in-Flight Orientation to Plant and Plant–Host Complex Volatiles inAphidius erviHaliday (Hymenoptera, Braconidae)

The effect of adult experience on in-flight orientation to plant–host complex volatiles byAphidius erviHaliday was studied in a wind tunnel bioassay, usingAcyrthosiphon pisum(Harris), maintained on broad bean plants (Vicia faba) as host. A short oviposition experience (15 s) on the plant–host complex (PHC) was sufficient to induce a drastic decrease of flight propensity and stimulated a foraging behavior characterized by intense walking activity. However, flight activity resumed to normal levels 1 h after the oviposition experience on the PHC occurred. For parasitoids conditioned on the PHC for at least 1 min the recorded proportion making oriented flights to the PHC was significantly higher than that for naive females. In contrast, oviposition experience in the absence of plant material did not influence theA. erviflight response. Oviposition attempts on aphid dummies without egg release did not reduce flight activity. WhenA. ervifemales were exposed to glass beads coated withAc. pisumcornicle secretion, a priming effect was observed, resulting, compared with naive females, in a significantly higher rate of oriented flights to the PHC. In contrast, oviposition attempts visually induced by colored aphid dummies did not influence flight behavior. A strong reaction to volatile cues from uninfested plants was induced by oviposition experience on newly infested broad bean plants. This appears to be a case of associative learning. In fact, uninfested broad bean plants are basically unattractive to naiveA. ervifemales. The results demonstrate that adult experience has a considerable influence onA. ervibehavior and may have important implications for biological control of natural pest aphid populations.     

Does variation in host plant association and symbiont infection of pea aphid populations induce genetic and behaviour differentiation of its main parasitoid, Aphidius ervi?

The host-associated differentiation (HAD) hypothesis states that higher trophic levels in parasitic associations should exhibit similar divergence in case of host sympatric speciation. We tested HAD on populations of Aphidius ervi the main parasitoid of the pea aphid Acyrthosiphon pisum, emerging from host populations specialized on either alfalfa or red clover. Host and parasitoid populations were assessed for genetic variation and structure, while considering geography, host plant and host aphid protective symbionts Regiella insecticola and Hamiltonella defensa as potential covariables. Cluster and hierarchical analyses were used to assess the contribution of these variables to population structure, based on genotyping pea aphids and associated A. ervi with microsatellites, and host aphid facultative symbionts with 16S rDNA markers. Pea aphid genotypes were clearly distributed in two groups closely corresponding with their plant origins, confirming strong plant associated differentiation of this aphid in North America. Overall parasitism by A. ervi averaged 21.5 % across samples, and many parasitized aphids producing a wasp hosted defensive bacteria, indicating partial or ineffective protective efficacy of these symbionts in the field. The A. ervi population genetic data failed to support differentiation according to the host plant association of their pea aphid host. Potential for parasitoid specialization was also explored in experiments where wasps from alfalfa and clover aphids were reciprocally transplanted on alternate hosts, the hypothesis being that wasp behaviour and parasitic stages should be most adapted to their host of origin. Results revealed higher probability of oviposition on the alfalfa aphids, but higher adult emergence success on red clover aphids, with no interaction as expected under HAD. We conclude that our study provides no support for the HAD in this system. We discuss factors that might impair A. ervi specialization on its divergent aphid hosts on alfalfa and clover.     

The use of visual cues in host evaluation by aphidiid wasps I. Comparison between threeAphidius parasitoids of the pea aphid

Host evaluation behaviour was examined in three species of aphid parasitoids,Aphidius ervi haliday,A. pisivorus Smith, andA. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae). Parasitoids were provided under laboratory conditions with three kinds of hosts representing two aphid species: (green) pea aphid,Acyrthosiphon pisum (Harris), and green and pink colour morphs of the alfalfa aphid,Macrosiphum creelii Davis. Females of all threeAphidius species distinguished between aphids on the basis of colour, movement, and host species. Patterns of host acceptance by parasitoids were species-specific. InA. ervi, host preference was the same in light and dark conditions: pea aphid>green alfalfa aphid≫pink alfalfa aphid. In contrast,A. pisivorus attacked and accepted pea aphid and green alfalfa aphid equally in the light and preferred both of these over pink alfalfa aphid; however, it made no distinction between pea aphid and pink alfalfa aphid in the dark. Females ofA. smithi attacked all three kinds of hosts (pea aphid>green alfalfa aphid≫pink alfalfa aphid) but apparently laid eggs only in pea aphid. The frequencies of attack and oviposition by all wasps were higher on ‘normal’ pea aphids than on those anaesthetized with CO₂. Host recognition is confirmed by chemical cues in the aphid cuticle that are detected during antennation, and host acceptance is dependent on an assessment of host quality during ovipositor probing.     

The influence of light environment on host colour preference in a parasitoid wasp

1. Visual chromatic cues and contrast effects are widely used by insects in behaviours involving host/prey/mate‐finding and recognition. However, naturally changing light conditions may challenge the visual perception of cues for these organisms. 2. We used the host/parasitoid system Acyrthosiphon pisum/Aphidius ervi to determine if apparent visual preference of the wasp for green over pink host aphids was a visually based choice or a post‐attack mechanism based on host susceptibility depending on anti‐parasitoid symbiotic bacteria. 3. The study tested the ability of the wasp to recognise and attack pea aphid clones expressing variation based on colour and/or symbionts under a broad range of LED‐controlled light environments mimicking natural variations. 4. Results showed that the amount of reflected light of pink morphs was about half that of the green morphs in the cyan‐green components. Both host colours were recognised and attacked under all tested light conditions, even red light (660 nm). The previously reported preference of A. ervi for green pea aphids, was clear only for naive females given a choice between two aphid colours under all light environments, but quickly disappeared. 5. Wasps showed no tendency of avoiding oviposition in clones with defensive symbionts. 6. These findings suggest that variable rates of pea aphid parasitism by A. ervi in fields do not depend on host colour discrimination, but rather on susceptibility variation among aphid clones in allowing larval development after egg‐laying. Further studies should consider deeper investigation of the impact of red lights used in modified light environments in greenhouses and the proportion of host colour morph available.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.