Encounters between aphids and their predators: the relative frequencies of disturbance and consumption

Ecologists may wish to evaluate the potential for predators to suppress prey populations through the costs of induced defensive behaviors as well as through consumption. In this paper, we measure the ratio of non‐consumptive, defense‐inducing encounters relative to consumptive encounters (henceforth the ‘disturbed : consumed ratio’) for two species of aphids and propose that these disturbed : consumed ratios can help evaluate the potential for behaviorally mediated prey suppression. For the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was high, 30 : 1. For the cotton aphid, Aphis gossypii (Glover) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was low, approximately 1 : 14. These results indicate that the potential for predators to suppress pea aphid populations through induction of defensive behaviors is high, whereas the potential for predators to suppress cotton aphid populations through induced behaviors is low. In measuring the disturbed : consumed ratios of two prey species, this paper makes two novel points: it highlights the variability of the disturbed : consumed ratio, and it offers a simple statistic to help ecologists draw connections between predator–prey behaviors and predator–prey population dynamics.     

Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Fly disturbance suppresses aphid population growth

1. The presence of predators is known to suppress prey populations not only by consumptive but also by non-consumptive effects, as it stresses the prey inducing costly changes to behaviour and physiology. However, there is recent evidence that disturbance from non-predacious, non-competing commensals can also negatively affect herbivore performance. 2. Populations of cherry-oat aphids (Rhopalosiphum padi L.) were initiated with adult aphids in mesocosms containing seedling wheat grass. Following aphid establishment, fruit flies (Drosophila melanogaster Meigen) were added at a relatively high density to half of the mesocosms and the aphids were left for another 5 days to reproduce. The experiment was performed over two blocks at 24 ± 4 °C. It was hypothesized that a relatively high density of commensals would stress the aphids and reduce their fitness, causing lower population growth and resulting in lower population sizes. 3. Aphid numbers were significantly lower in mesocosms with commensal flies after 5 days of fly presence across the two experimental blocks, documenting that fly disturbance suppresses aphid fitness and population growth. 4. The negative effect of fruit flies on aphid population growth must have come from the disturbance that flies imposed on the aphids in their search for food, indicating that the flies stressed the aphids. Thus, our study indicates that commensals may stress herbivores that do not distinguish between enemies and other active species in their environment, adding in the overall herbivore top-down control through fitness costs.     

Syrphid flies suppress lettuce aphids

Syrphid flies are abundant in lettuce fields, where their larvae are key predators of aphids. However, the presence of predators in the field does not always result in economically significant levels of prey suppression. Even when predators are numerous, their effects on prey population dynamics may be variable. Over a two year period we surveyed lettuce fields in coastal California, USA to test whether syrphid flies are capable of colonizing fields with aphids and suppressing aphid population growth. The survey showed that female syrphids oviposited more eggs at locations with more aphids, and that greater numbers of syrphid larvae resulted in lower rates of increase in the aphid populations. We also directly manipulated syrphid densities by adding syrphid eggs to uncaged lettuce plants, and these syrphid additions resulted in lower aphid population growth. This research shows that syrphid flies have the ability to suppress aphid populations in lettuce fields.     

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.     

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.     

Potential cotton aphid,Aphis gossypii,population suppression by arthropod predators in upland cotton

The cotton aphid, Aphis gossypii Glover, predation rate of convergent lady beetle, Hippodamia convergens Guerin‐Meneville, was determined by assigning a single predator randomly to each of four prey density treatments in the laboratory. Prey densities included 25, 50, 100, and 200 aphids per Petri dish arena. Predation response was recorded at 1, 4, 8, 16, 24, and 48 h after assigning predators to their prey treatments. Rate of consumption increased through time, with all 25 aphids consumed during the first 4 h of the experiment. At the highest density, adult lady beetle consumed on average 49, 99, 131, 163, 183, and 200 aphids within 1, 4, 8, 16, 24 and 48 h, respectively. Predators showed a curvilinear feeding response in relation to total available time, indicating that convergent lady beetles have the potential to suppress larger populations of aphids through continuous feeding by regulating their predation efficiency during feeding. The analysis of age‐specific mortality in absence of prey revealed that lady beetles could survive for an extended period of time (more than 2 weeks) without prey. The ability of a predator to survive without prey delays or prevents the rebound of pest populations that is a significant factor in natural biological control. A two‐year field sampling of 10 cotton arthropod predator species showed that spiders (27%) were the most dominant foliage dwelling predators in the Texas High Plains cotton followed by convergent lady beetles (23.5%), hooded beetles (13.5%), minute pirate bugs (11%), green lacewings (9.5%), bigeyed bugs (7.5%), scymnus beetles (3%), soft‐winged flower beetles (2%), damsel bugs (1.5%), and assassin bugs (1.5%). A field cage study showed that one H. convergens adult per plant released at prey density of one aphid per leaf kept the aphid population below economic threshold for the entire growing season.     

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.     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Comparison of native and non‐native predator consumption rates and prey avoidance behavior in North America and Europe

Novel predator–prey interactions can contribute to the invasion success of non‐native predators. For example, native prey can fail to recognize and avoid non‐native predators due to a lack of co‐evolutionary history and cue dissimilarity with native predators. This might result in a competitive advantage for non‐native predators. Numerous lady beetle species were globally redistributed as biological control agents against aphids, resulting in novel predator–prey interactions. Here, we investigated the strength of avoidance behavior of the pea aphid (Acyrthosiphon pisum) toward chemical cues of native lady beetles and non‐native Asian Harmonia axyridis and European Coccinella septempunctata and Hippodamia variegata in North America, hypothesizing that cues of non‐native lady beetles induce weaker avoidance behavior than cues of co‐evolved native lady beetles. Additionally, we compared aphid consumption of lady beetles, examining potential predation advantages of non‐native lady beetles. Finally, we compared cue avoidance behavior between North American and European pea aphid populations and aphid consumption of native and non‐native lady beetles in North America and Europe. In North America, pea aphids avoided chemical cues of all ladybeetle species tested, regardless of their origin. In contrast to pea aphids in North America, European pea aphids did not avoid cues of the non‐native H. axyridis. The non‐native H. axyridis and C. septempunctata were among the largest and most voracious lady beetle species tested, on both continents. Consequently, in North America non‐native lady beetle species might have a competitive advantage on shared food resources due to their relatively large body size, compared to several native American lady beetle species. In Europe, however, non‐native H. axyridis might benefit from missing aphid cue avoidance as well as a large body size. The co‐evolutionary time gap between the European and North American invasion of H. axyridis likely explains the intercontinental differences in cue avoidance behavior and might indicate evolution in aphids toward non‐native predators.     

Interspecific symbiont transfection confers a novel ecological trait to the recipient insect

In Japan, pea aphids Acyrthosiphon pisum mainly feed on vetch and clover, and many aphid clones produce more progeny on vetch than on clover. In this context, particular genotypes of the facultative symbiont Regiella insecticola enhance reproduction of infected pea aphids specifically on clover, thereby broadening the suitable food plant range of the insect. A species that is sympatric to A. pisum, vetch aphids Megoura crassicauda, are commonly found on vetch but not on clover. Laboratory rearing of M. crassicauda strains revealed active reproduction on vetch but substantially no reproduction on clover. Experimental transfection of Regiella from A. pisum to M. crassicauda by haemolymph injection established stable and heritable infection in the recipients, although no Regiella infection has been detected in natural populations of M. crassicauda. Different strains of Regiella-transfected M. crassicauda grew and reproduced on vetch, but exhibited lower fitness in comparison with corresponding uninfected aphid strains. Strikingly, the Regiella-transfected M. crassicauda exhibited improved survival and some reproduction on clover. These results suggest that Regiella has the potential to confer an ecological trait, adaptation to clover, on novel insect hosts, and also account for why Regiella is able to infect M. crassicauda but is scarcely found in these aphid populations.     

Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions

Generalist insect predators can significantly impact the dynamics of pest populations; and, using alternative prey, they can rapidly establish in disturbed agroecosystems. However, indirect interactions between prey can occur, leading to either increased or decreased predation on focal prey. The present paper demonstrates how alternative prey can disrupt predation by the hemipteran Orius insidiosus on the soybean aphid Aphis glycines via short-term indirect interactions. We used laboratory microcosms to measure the impact of the predator on the population growth of the aphid in the presence of alternative prey, soybean thrips Neohydatothrips variabilis, and we characterized the foraging behaviour of the predator to assess prey preference. We showed that O. insidiosus predation on aphids was reduced in the presence of thrips and that this positive impact on aphids increased as thrips density increased. Results from the behavioural experiment support the hypothesis of a prey preference toward thrips. When prey-pest ratio is aphid-biased, short-term apparent commensalism between prey occurs in favour of the most abundant prey (aphids) with no switching behaviour appearing in O. insidiosus. These results demonstrate that potential indirect interactions should be taken into account when considering O. insidiosus as a biocontrol agent against the soybean aphid.     

Life history characteristics of Orius insidiosus (Say) fed diets of soybean aphid, Aphis glycines Matsumura and soybean thrips, Neohydatothrips variabilis (Beach)

Field studies in soybeans have demonstrated that the endemic predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid, Aphis glycines Matsumura. Soybean thrips, Neohydatothrips variabilis (Beach), serve as an important prey resource for O. insidiosus in soybeans and may be important in sustaining O. insidiosus populations before the arrival of soybean aphid. Because soybean aphid is new to the US soybean system, the effects of a mixed diet of soybean aphid and soybean thrips on O. insidiosus life history is not known. We measured the survival, development, and reproduction of O. insidiosus when fed soybean thrips, and a mixed prey diet of soybean aphids and soybean thrips, and compared these results to a previous study of O. insidiosus life history fed soybean aphid alone. Nymphal development to adulthood (15.9 days) and fecundity (68.8 eggs per female) was improved for O. insidiosus fed ad libitum soybean thrips daily compared to O. insidiosus fed ad libitum soybean aphids daily. The contribution of alternative prey to O. insidiosus life history characteristics can be complex depending on the amount and quality of a particular prey item. At low levels of prey, the addition of prey appears to enhance O. insidiosus survival, development, and fecundity. However, as predators are fed more often, the predator’s response depends on the type of prey that predominates in the mixed prey diet. We discuss soybean thrips impact on O. insidiosus population ecology and soybean aphid dynamics.     

Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids,Acyrthosiphon pisum (Hemiptera: Aphididae)

1. Aphid natural enemies include not only predators and parasitoids but also pathogens, of which fungi are the most studied for biological control. While wing formation in aphids is induced by abiotic conditions, it is also affected by biotic interactions with their arthropod natural enemies. Wing induction via interactions with arthropod natural enemies is mediated by the increase in their physical contact when alarmed (pseudo‐crowding). Pathogenic fungi do not trigger this alarm behaviour in aphids and, therefore, no pseudo‐crowding occurs. 2. We hypothesise that, while pathogenic fungi will stimulate maternally induced wing formation, the mechanism is different and is influenced by pathogen specificity. We tested this hypothesis using two entomopathogenic fungi, Pandora neoaphidis and Beauveria bassiana, an aphid specialist and a generalist respectively, on the pea aphid, Acyrthosiphon pisum Harris. 3. We first demonstrate that pea aphids infected with either pathogen and maintained in groups on broad bean plants produced a higher proportion of winged morphs than uninfected control aphids. We then show that, when maintained in isolation, aphids infected with either pathogen also produced higher proportions of winged offspring than control aphids. There was no difference between P. neoaphidis and B. bassiana in their effects on wing induction in either experiment. 4. Unlike the effect of predators and parasitoids on pea aphid wing induction, the effect of pathogens is independent of physical contact with other aphids, suggesting that physiological cues induce wing formation in infected aphids. It is possible that aphids benefit from wing induction by escaping infected patches whilst pathogens may benefit through dispersion. Possible mechanisms of wing induction are discussed.     

Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey

Generalist predators are potential controlagents of aphids in cereal fields. Becauseaphids are low-quality prey for most generalistpredators, the availability of alternativehigh-quality prey may influence theinteractions between aphids and their predatorsby reducing the predation rate due to loweredpreference for aphids. We analysed this bytesting the ability of six generalist predators(the spiders Erigone atra (Bl.), Clubiona lutescens (Westr.)/reclusaO.P.-C., Pachygnatha degeeri Sundevall,Pardosa prativaga (L.Koch), the carabidbeetle Bembidion lampros (Herbst), andthe harvestman Oligolophus tridens (C.L.Koch)) to suppress Rhopalosiphum padi(Linné) populations in the presence orabsence of alternative prey types (fruit fliesDrosophila melanogaster (Meigen) or thecollembolan Tomocerus bidentatus(Folsom)). Experiments of 10 days duration werecarried out in a microcosm set-up. Withoutalternative prey all predators except B.lampros were able to reduce aphid populationdevelopment significantly relative topredator-free controls. The harvest spider O. tridens was the most efficient predator(<90% reduction). Presence of alternativeprey (fruit flies) had a significant negativeeffect on aphid limitation by P. prativagaand a weak positive effect in B. lampros, but did not influence the ability to reduce aphids in E. atra, Clubiona, P. degeeri and O. tridens. In addition, 24-hours' consumption experiments with adult P. degeeri and subadult C. lutescens/reclusa, using R. padi and D. melanogaster as prey types, showed markedly lower consumption rates of aphid than of fruit fly prey. The microcosm arrangement is a simple way to partly simulate the habitat complexity of an agricultural field under laboratory conditions and proved to be a useful tool for investigating complex predator-prey interactions.     

Predator-induced morphological shift in the pea aphid

Aphids exhibit a polymorphism whereby individual aphids are either winged or unwinged. The winged dispersal morph is mainly responsible for the colonization of new plants and, in many species, is produced in response to adverse environmental conditions. Aphids are attacked by a wide range of specialized predators and predation has been shown to strongly influence the growth and persistence of aphid colonies. In two experiments, we reared two clones of pea aphid (Acyrthosiphon pisum) in the presence and absence of predatory ladybirds (Coccinella septempunctata or Adalia bipunctata). In both experiments, the presence of a predator enhanced the proportion of winged morphs among the offspring produced by the aphids. The aphid clones differed in their reaction to the presence of a ladybird, suggesting the presence of genetic variation for this trait. A treatment that simulated disturbance caused by predators did not enhance winged offspring production. The experiments indicate that aphids respond to the presence of a predator by producing the dispersal morph which can escape by flight to colonize other plants. In contrast to previous examples of predator-induced defence this shift in prey morphology does not lead to better protection against predator attack, but enables aphids to leave plants when mortality risks are high.     

Impact of abiotic factors on predator-prey interactions: DNA-based gut content analysis in a microcosm experiment

The effects of predators on prey populations can be modified by a number of abiotic factors. Here, we investigated the combined and separate effects of rain and ground-dwelling predators on aphid populations in a microcosm experiment lasting for 21 days, using PCR to analyse the gut content of the predators. Rain significantly dislodged aphids from shoots and ears by 57% and 25%, respectively. The gut content analysis showed that more predators consumed aphids in the rain treatment than without rain, indicating higher availability of aphids to ground-dwelling predators after rain. However, no synergistic effects of rain and ground-dwelling predators on aphid population development could be demonstrated. Rain alone significantly decreased aphid populations by 27%, suggesting that this is a significant mortality factor. Predators alone had no significant effect on aphid numbers, but the gut content analyses showed aphid consumption also in the no-rain treatments, indicating that aphids were available to the predators on the soil surface even without rain. Our results suggest that weather conditions such as rain can modify predator-prey interactions in the field. Employing PCR-based predator gut content analyses proved to be useful as trophic links could be directly verified.     

Temporal habitat variability and the maintenance of sex in host populations of the pea aphid

The evolutionary maintenance of sex, despite competition from asexual reproduction, has long intrigued the evolutionary biologists owing to its numerous apparent short-term costs. In aphids, winter climate is expected to determine the maintenance of sexual lineages in the high latitude zones owing to their exclusive ability to produce frost-resistant eggs. However, diverse reproductive modes may coexist at a local scale where climatic influence is counteracted by microgeographical factors. In this study, we tested the influence of local habitat characteristics on regional coexistence of reproductive modes in the pea aphid, Acyrthosiphon pisum. In the laboratory, the induction of sexual morph production of many pea aphid genotypes from the local fields of annual (pea and faba bean) and perennial (alfalfa and red clover) crops in Western France indicated that A. pisum lineages from annual crops had a significantly higher investment in sexual reproduction than A. pisum lineages from the perennial hosts. We propose that temporal habitat variability exerts a selective pressure to maintain the sexual reproduction in A. pisum. The ecological and evolutionary consequences of the association between the mode of reproduction and the host population on gene flow restriction and on ecological specialization are discussed.     

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.     

Alate immigration disrupts soybean aphid suppression by predators

Natural enemies suppress many aphid populations, and yet, population outbreaks sometimes occur. The reasons predation fails to suppress such outbreaks are not clearly understood. While manipulating predators to examine their role in soybean aphid population growth, a natural immigration of soybean aphids occurred that enabled us to compare the roles immigration and predation played in population growth. Using predator exclusion cages, we found that predation on the top of the plant accounted for 42.3 ± 11.4% (mean ± SE) reduction in aphid population growth rates. When 90–100% of the canopy was exposed, predation failed to reduce aphid population growth because winged immigrants colonized plants, with an observed 6‐fold increase in alates compared to plants completely covered or exposing only the top nodes (approximately 10% of the total canopy). We conclude that reproduction by immigrants contributed to population growth rates sufficiently to compensate for predation. These results demonstrate that immigration can counteract high levels of predation and lead to aphid population growth rates that could result in outbreak population densities.