Clumped distribution patterns in goldenrod aphids: genetic and ecological mechanisms

Abstract.

• 1 The aphids Uroleucon tissoti and U.nigrotuberculatum both exhibit significantly aggregated distribution patterns across clumps of their common host plant Solidago altissima, the tall goldenrod. However, U.nigrotuberculatum is significantly more aggregated than is U.tissoti. We tested the hypothesis that goldenrod genotype-by-U.tissoti genotype interactions for aphid performance characters could partially account for this difference.
• 2 Only one of the characters we measured showed a significant genotype-bygenotype interaction; therefore it is unlikely that such interactions affect the distribution of U.tissoti across goldenrod stems.
• 3 In addition, we found that three environmental variables (genetic variation for resistance to herbivory, host plant morphology, and local host density) affect the degree of aggregation found in both U.tissoti and U.nigrotuberculatum populations.

     

Alterations in foraging behavior of Coccinella septempunctata and Propylea japonica mediated by a novel defended prey affect their predatory potential

Generalist aphidophagous coccinellids have to cope with novel prey aphids in environments that are changing rapidly because of anthropogenic activity. The goldenrod aphid, Uroleucon nigrotuberculatum (Olive) (Hemiptera: Aphididae), is a noxious prey, which was recently introduced into Japan. It is a major prey for the native Japanese predators Coccinella septempunctata bruckii Mulsant and Propylea japonica (Thunberg) (both Coleoptera: Coccinellidae) in early summer on patches of solidago, Solidago altissima L. (Asteraceae). Prey preference of these coccinellids between this aphid and a native suitable prey aphid, Megoura crassicauda Mordvilko (Hemiptera: Aphididae), as well as their foraging behavior were studied for a better understanding of the negative impacts of the noxious novel aphid. Coccinella septempunctata initially preferred the novel prey, but later switched to the native prey, M. crassicauda; P. japonica had no preference for either prey. Feeding time of the first instars of C. septempunctata on U. nigrotuberculatum was significantly longer than that of P. japonica. The foraging bouts of fourth instars of C. septempunctata were significantly longer on U. nigrotuberculatum than on M. crassicauda, whereas only the feeding time of fourth instars of P. japonica on U. nigrotuberculatum was significantly longer than on M. crassicauda. Both coccinellids consumed less of U. nigrotuberculatum than of M. crassicauda. Thus, solidago patches infested by U. nigrotuberculatum may present an ecological trap, especially for C. septempunctata.     

APHID DISTRIBUTION AND THE EVOLUTION OF GOLDENROD RESISTANCE

Although there is considerable evidence indicating that herbivory is detrimental to plant fitness, some recent studies of the evolution of plant resistance have concluded that insects do not impose selection on their host plants. A previously untested assumption that underlies most studies of the evolution of plant resistance is that insect distribution patterns are controlled directly by the effects of plant genotype on insect preference and performance. The experiments described here explicitly tested this assumption using the specialist herbivore Uroleucon tissoti (Homoptera: Aphididae) and its host plant Solidago altissima (Asteraceae). Measures of aphid preference and performance were used to predict aphid distribution patterns, and then the predicted distribution patterns were compared with the natural distribution pattern. Although goldenrod genotype had a strong effect on aphid distribution, aphid distribution was not controlled directly by the effect of goldenrod genotype on aphid preference and performance. Instead, a second experiment demonstrated that aphid and spittlebug (Philaenus spumarius and Lepyronia quadrangularis Homoptera: Cercopidae) distribution is controlled largely by genetic variation for resistance to a suite of “branch-causing” herbivores. These herbivores induce branching and aphids and spittlebugs are more abundant on branched plants than unbranched plants. These results indicate that any natural selection imposed by aphids and spittlebugs on goldenrod will depend on the presence or absence of branch-causing herbivores. Thus, selection for plant resistance may depend as much on the assemblage of insect species present as on the identity of each individual species.     

Response by coccinellids to spatial variation in cereal aphid density

The objectives of this study were to determine if coccinellids adjusted their distribution within spring wheat fields in response to spatial variation cereal aphid density in the fields and to describe the patterns of cereal aphid population growth that resulted. Field experiments were completed in which the physical dimensions of patches infested with cereal aphids, cereal aphid density, and access to patches by coccinellids were varied. Aphid infestations consisted of naturally occurring densities (natural patches) and much greater densities created by supplementing patches with aphids (supplemented patches). Coccinellids were denied access to some supplemented patches (exclusion patches) but allowed unlimited access to others. Densities of adult Hippodamia convergens and Coccinella septempunctata were correlated with aphid density in patches whereas density of Coleomegilla maculata was not. Aggregation by coccinellids was independent of patch area. The realized aphid population growth rate (r) was lower in supplemented than natural patches in all four trials but was significantly lower in only one trial. The lower r in supplemented patches was not exclusively caused by coccinellid predation, and emigration of aphids from patches probably also contributed. r was significantly greater in exclusion patches than supplemented and natural patches, indicating that coccinellids markedly reduced aphid numbers in patches even when aphid density was extremely high. Received: February 17, 1999 / Accepted: February 1, 2000     

Community‐wide impact of an exotic aphid on introduced tall goldenrod

1. The aphid Uroleucon nigrotuberculatum Olive, which is specialised to the tall goldenrod, Solidago altissima L., in its native range, has become a dominant species on the introduced tall goldenrod in Japan. How this exotic aphid influenced arthropod communities on the introduced tall goldenrod in aphid‐present (spring) and aphid‐absent (autumn) seasons was examined, using an aphid removal experiment. 2. In spring, aphid presence increased ant abundance because aphid honeydew attracted foraging ant workers. A significant negative correlation was found between the numbers of ants and herbivorous insects other than aphids on the aphid‐exposed plants, but no significant correlation was detected on the aphid‐free plants. Thus, the aphid presence was likely to decrease the abundance of co‐occurring herbivorous insects through removal behaviour of the aphid‐tending ants. There were no significant differences in plant traits between the aphid‐exposed and aphid‐free plants. 3. In autumn, the numbers of lateral shoots and leaves, and the leaf nitrogen content were increased in response to the aphid infestation in spring. Because of the improvement of plant traits by aphid feeding, the abundance of leaf chewers increased on aphid‐exposed plants. In contrast, the abundance of sap feeders decreased on the aphid‐exposed plants. In particular, the dominant scale insect among sap feeders, Parasaissetia nigra Nietner, decreased, followed by a decrease in the abundance of ants attending P. nigra. Thus, aphid feeding may have attenuated the negative impacts of the tending ants on leaf chewers. 4. Aphid presence did not change herbivore species richness but changed the relative density of dominant herbivores, resulting in community‐wide effects on co‐occurring herbivores through ant‐mediated indirect effects, and on temporally separated herbivores through plant‐ and ant‐mediated indirect effects. The aphid also altered predator community composition by increasing and decreasing the relative abundance of aphid‐tending ants in the spring and autumn, respectively.     

Ant- and plant-mediated indirect effects induced by aphid colonization on herbivorous insects on tall goldenrod

We studied the indirect effects of an aphid Uroleucon nigrotuberculatum on density and performance of herbivorous insects through tending ants and modification of plant traits on a tall goldenrod Solidago altissima in Japan. To examine ant-mediated indirect effects of the aphid on the leafhopper and geometrid moth caterpillars, we conducted an experiment in which we manipulated aphid densities. The aphid decreased the density of these herbivorous insects through ant-mediated indirect effects, because honeydew scattered by the aphid-attracted ants that then removed them. To examine plant-mediated indirect effects of the aphid on two temporally separated insects, a scale insect and a grasshopper, we compared the density and performance of these herbivorous insects on aphid-inoculated plants and aphid-free plants. Aphid-induced plant modifications had different effects on the scale insect and grasshopper. The aphid indirectly decreased the density and survivorship of the scale insect. On the other hand, the number of grasshoppers increased as a result of the increased number of leaves and the increased nitrogen content induced by prior aphid feeding. However, aphid infestation did not affect the survival of the grasshopper. Thus, the aphid has large indirect effects on co-occurring herbivorous insects through the removal behavior of tending ants and on temporally separated herbivorous insects through changes in quality and quantity of the tall goldenrod.     

Monoclonal antibodies reveal changes in predator efficiency with prey spatial pattern

Spatially explicit predator–prey interactions can alter the predatory potential of natural enemies augmented through conservation biological control. To test hypotheses regarding such interactions and predatory efficiency, we used a combination of molecular techniques and mark–release–recapture to study the foraging behaviour of a generalist carabid predator, Poecilus cupreus , in response to spatial patterns of its cereal aphid prey ( Metapolophium dirhodum and Sitobion avenae ). Beetle and aphid numbers were measured across two grids of sampling locations, within which aphid spatial pattern had been manipulated to generate patchy and more homogenous distributions. Aphid consumption was measured by enzyme-linked immunosorbent assays (ELISA) of beetle gut contents, using an aphid-specific monoclonal antibody. Movement and distribution patterns suggest that P. cupreus does not aggregate at, nor instigate prey-taxis within, aphid patches. However, more than two-thirds of the 2169 P. cupreus tested by ELISA had consumed aphids and the proportion of beetles containing aphid proteins was positively related to aphid density. Against expectation, the proportion of predators feeding on aphids was greatest where prey were homogenously distributed, and this was attributed to the loss of partial refuges for prey in aphid patches. The functional value of this type of uniform foraging strategy is ideally suited to early colonization of the crop habitat, when aphid numbers are low, before populations build up and form strong spatial patterns.     

The oviposition behavior ofAphidius ervi andMonoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches

Two-day-old mated females ofAphidius ervi Haliday andMonoctonus paulensis (Ashmead) were each provided with two sequential host patches. Patches were comprised of plastic petri dishes containing either 15 pea aphids,Acyrthosiphum pisum (Harris), or 15 alfalfa aphids,Macrosiphum creelii Davis. Both wasp species parasitized more hosts in patches containing pea aphids than in those containing alfalfa aphids, regardless of sequence. Females ofA. ervi also laid more eggs per aphid in patches containing pea aphids than in patches containing alfalfa aphids. When both patches contained alfalfa aphids,M. paulensis females parsitized more aphids in the second patch than in the first. Fewer alfalfa aphids were parasitized in the second patch when the first patch contained pea aphids, and fewer eggs were laid per alfalfa aphid. Parasitoid females of both species exhibited consistently higher rates of oviposition into their preferred host species and adjusted their reproductive allocation to hosts and host patches as a function of their experience in previous patches.     

Transgenerational phenotypic plasticity under future atmospheric conditions

Organisms often exhibit transgenerational phenotypic changes in response to an increased risk of parasitism or predation. Shifts in global atmospheric composition could modify these phenotypic effects through changes in either nutrient quantity/quality or altered interactions with higher trophic levels. Here we show that future atmospheric conditions alter a natural enemy‐induced wing polyphenism in aphids. Winged offspring production by Uroleucon nigrotuberculatum aphids on goldenrod (Solidago canadensis var. scabra) does not differ in enriched CO₂ and/or O₃ atmospheres. However, proportionally more winged offspring are produced in response to search cues from both coccinellid predators (Coccinella septempunctata) and hymenopteran parasitoids (Aphidius polygonaphis) relative to plants not searched by natural enemies. Moreover, the magnitude of this response differs under enriched CO₂ and O₃ environments. Aphids produce more winged offspring in response to predators under elevated CO₂, but produce more winged offspring in response to parasitoids under elevated O₃. Thus, global atmospheric changes influence natural enemy‐mediated phenotypic expression, with potentially far‐reaching consequences for trophic dynamics.     

Cornicle secretions of Uroleucon nigrotuberculatum (Homoptera: Aphididae) as the last bullet against lady beetle larvae

Aphids have evolved various defense strategies against natural enemies, including secretions from their cornicles. We assessed the defensive function of cornicle secretions by the goldenrod aphid, Uroleucon nigrotuberculatum (Olive), against larvae of the lady beetles Coccinella septempunctata bruckii Mulsant and Propylea japonica (Thunberg) (Coleoptera: Coccinellidae). The aphid secreted red droplets from its cornicles when attacked by the larvae. Two‐thirds of the C. septempunctata bruckii larvae and 46.7% of the P. japonica larvae that preyed on the aphids died before reaching the pre‐pupal stage. The secretions caused molting failure when smeared on the larvae's heads or glued to the larvae's mouthparts, killing 56.7% of C. septempunctata bruckii larvae and 36.7% of P. japonica larvae. Second instar larvae were affected most. About 40% of third and fourth instar larvae of C. septempunctata bruckii vomited soon after ingesting the aphids. In the field, up to 40% of first and second instar larvae were smeared with red secretions. Our results show that these cornicle secretions are an effective and active defense against earlier instars of coccinellid larvae.     

Native primary parasitoids and hyperparasitoids attacking an invasive aphid Uroleucon nigrotuberculatum in Japan

Since the invasion of Uroleucon nigrotuberculatum from North America we searched for parasitoids of this aphid on Solidago altissima in Japan to determine what species of native parasitoids attack the newly invasive aphid. We found three primary parasitoid species: Ephedrus plagiator and Praon yomenae (Braconidae, Aphidiinae) and Aphelinus albipodus (Aphelinidae). We also found eight hyperparasitoid species: Syrphophagus sp. (Encyrtidae), Dendrocerus carpenteri (Megaspilidae), Asaphes suspensus (Pteromalidae) and Pachyneuron aphidis (Pteromalidae) through both E. plagiator and A. albipodus; Phaenoglyphis villosa (Figitidae, Charipinae), Aprostocetus sp. (Eulophidae, Tetrastichinae) and D. laticeps through E. plagiator, and Alloxysta sp. nr brevis (Figitidae, Charipinae) through A. albipodus. Uroleucon nigrotuberculatum is usually attacked by rather polyphagous primary parasitoids, E. plagiator and A. albipodus, in Japan, where an oligophagous parasitoid specialized to allied aphid species is probably absent. The hyperparasitoid community of U. nigrotuberculatum is common to those of the aphids occurring in open field‐type habitats in Japan.     

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.     

The spatial distribution of canopy-resident and ground-resident cereal aphids (Sitobion avenae and Metopolophium dirhodum) in winter wheat

We investigated, within two cereal fields in Southern England, the within-canopy spatial distribution of the aphids Sitobion avenae and Metopolophium dirhodum in relation to crop yield and plant nitrogen. We extended the study to investigate the spatial distribution of aphids that fell to, or returned from, the ground in order to estimate availability of the within-canopy aphid population to ground-active predators. We revealed that crop canopy aphid spatial pattern was associated with nitrogen or yield. Differences were evident between species: S. avenae was generally negatively associated with yield or plant nitrogen, whilst M. dirhodum exhibited positive association. For both aphid species, we observed strong spatial pattern for aphids falling to the ground and conclude that this could, in part, mediate the effectiveness of ground-active predators as pest control agents.     

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

1. While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators.
2. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis.
3. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis.
4. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator.
5. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.

     

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.     

Aggregation of polyphagous predators in response to multiple prey: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa

The spatial distribution of polyphagous predators may often reflect the integration of aggregative responses to local densities of multiple species of prey, and as such may have consequences for the indirect linkages among the prey sharing these predators. In a factorial field experiment in which we manipulated local prey densities within a field of alfalfa in Utah (USA), we tested whether aphidophagous ladybirds would aggregate not only in response to their primary aphid prey, but also in response to an abundant alternative prey, the alfalfa weevil (Hypera postica [Gyllenhal]). Native North American ladybirds (primarily Hippodamia convergens Guerin and H. quinquesignata quinquesignata [Kirby]) responded only to spatial variation in aphid density. In contrast, the introduced ladybird, Coccinella septempunctata L., aggregated also at local concentrations of the weevil late in the experiment when weevil density was high and aphid density was relatively low throughout all experimental plots. The results support the hypothesis that C. septempunctata is more responsive than are native ladybirds to the availability of alternative prey in alfalfa, which may account in part for the displacement of native ladybirds from alfalfa by the introduced species as aphid numbers have declined. The differing responses of the native and introduced ladybirds to spatial patterns of the alternative prey underscore the importance of extending the study of predator aggregation to understand better how polyphagous predators distribute themselves in response to spatial patterns of multiple species of potential prey.     

Coexistence through mutualist‐dependent reversal of competitive hierarchies

Mechanisms that allow for the coexistence of two competing species that share a trophic level can be broadly divided into those that prevent competitive exclusion of one species within a local area, and those that allow for coexistence only at a regional level. While the presence of aphid‐tending ants can change the distribution of aphids among host plants, the role of mutualistic ants has not been fully explored to understand coexistence of multiple aphid species in a community. The tansy plant (Tanacetum vulgare) hosts three common and specialized aphid species, with only one being tended by ants. Often, these aphids species will not coexist on the same plant but will coexist across multiple plant hosts in a field. In this study, we aim to understand how interactions with mutualistic ants and predators affect the coexistence of multiple species of aphid herbivores on tansy. We show that the presence of ants drives community assembly at the level of individual plant, that is, the local community, by favoring one ant‐tended species, Metopeurum fuscoviride, while preying on the untended Macrosiphoniella tanacetaria and, to a lesser extent, Uroleucon tanaceti. Competitive hierarchies without ants were very different from those with ants. At the regional level, multiple tansy plants provide a habitat across which all aphid species can coexist at the larger spatial scale, while being competitively excluded at the local scale. In this case, ant mutualist‐dependent reversal of the competitive hierarchy can drive community dynamics in a plant–aphid system.     

Influence of the prey aphid Uroleucon nigrotuberculatum parasitizing Solidago canadensis on the larval and adult survivorship of the predatory ladybird beetle Harmonia axyridis

The ladybird beetle Harmonia axyridis is an aphidophagous natural enemy in Japan. The alien plant Solidago canadensis is widespread in Japanese agricultural landscapes, and the alien aphid Uroleucon nigrotuberculatum parasitizes the plant. We examined the quality of the aphid as food for all developmental stages of H. axyridis. First-instar larvae fed the aphid died within 2 days. Larvae at later developmental stages survived for significantly longer periods but died before pupation. Adults fed the aphid also died within 10 days. These results suggest that U. nigrotuberculatum parasitizing S. canadensis is unsuitable for H. axyridis during the beetle’s entire life cycle.     

The effect of rearing the ladybirdHarmonia axyridis onEphestia kuehniella eggs on the response of its larvae to aphid tracks

Larvae ofHarmonia axyridis Pallas (Col., Coccinellidae) exhibited two walking patterns during prey search. Extensive search occurred when searching for prey patches and was characterized by long linear paths and a fast speed. Intesive search, which appeared after the ingestion of a prey in a patch, resulted from a lowering of the linear speed and an increase in the number of stops and angular speed. When larvae reared on the aphidAcyrthosiphum pisum Harris (Hom., Aphidae) crossed an artificial substratum previously contaminated by this prey, they changed their path direction and adopted intensive search. They probably perceived aphid odor tracks and consequently modified their walking pattern. This gustatory capacity probably allowed very mobile larvae to locate prey patches more rapidly and improve encounter with preys in every patch.H. axyridis larvae reared on a substitute prey, the eggs ofEphestia kuehniella Zeller (Lep., Pyralidae), for more than a hundred generations, also changed their path orientation but retained extensive search. The weak response of these larvae to aphid tracks may have resulted from either a decrease in their sensitivity to gustatory aphid stimuli or their difficulty in associating aphid odor with aphid presence. These larvae needed more time and more preliminary encounters than larvae reared on aphids before catching prey.     

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.