Top-down and bottom-up effects on the spatiotemporal dynamics of cereal aphids: testing scaling theory for local density

The relationship between density and area depends on local growth rates and the area-dependence of migration rates. These rates vary among taxa due to dispersal behaviour, plot productivity and natural enemy impact. Previous studies in aphids suggest that aphid densities are highest in patches of intermediate sizes, and lower in small and large patches. The suggested mechanism causing these patterns is that the dispersal behaviour in aphids creates a mixture of area- and perimeter-dependent migration rates. In this paper, we used these predictions to examine the additional consequences of nutrient availability and natural enemies on the density-area relationship. The derived predictions were compared to data from a system with three aphid species, a set of aphid parasitoids and generalist natural enemies, and at two levels of plant nutrient availability. We find that predictions from the model based only on dispersal and local growth agree with the temporal dynamics of density-area relationships for aphids in high nutrient patches. In patches with low nutrients, high parasitism rates appeared to cause a negative density-area relationship for aphids, thereby deviating from predictions driven by the aphids' dispersal behavior. Hence, the dispersal model with scale-dependent migration rates can provide a useful tool for understanding insect distribution in patch size gradients, but the relative importance of top-down effects can completely change with plot productivity.     

Timing of dispersal: effect of ants on aphids

Mutualists can affect many life history traits of their partners, but it is unclear how this translates into population dynamics of the latter. Ant–aphid associations are ideal for studying this question, as ants affect aphids, both positively (e.g., protection against natural enemies) and negatively (e.g., reduction of potential growth rates). The unresolved question is whether these effects, which have been observed at the level of individuals and under controlled environmental conditions, have consequences at the population level. On estimating aerial aphid populations by using weekly suction trap data spanning up to 22 years from different locations in France, we show that in ant-attended aphid species long-distance dispersal occurs significantly later, but that the year-to-year changes in the peak number of migrants are not significantly lower than for non-attended aphids. Host alternation had the same retarding effect on dispersal as ant attendance. We discuss the delay in the timing of dispersal in ant-attended aphids, and potential costs that arise in mutualistic systems.     

A controlled environment study of the effect of leaf physiological age on the movement of apterous Myzus persicae on sugar-beet plants

Apterous Myzus persicae were found to move frequently from leaf to leaf on sugar-beet plants in controlled environment conditions. It is suggested that aphid movement can be related to changes in the rate and content of translocate flow during leaf development. These changes make newly-emerged leaves nutritionally favourable to colonising aphids and make expanding leaves slowly wane in favourability during the process of ‘sink to source’ conversion leading to aphid dispersal from the leaf. Variation in temperature was not found to alter the rate of aphid movement or the period (measured in thermal time) that aphids spent on particular leaves. However, the lower temperature was found to increase the rate of aphid development, aphid size and fecundity; these effects could also be due to nutritional factors. This dispersal behaviour may be a tactic to maximise food intake by a polyphagous aphid and increase the probability that nymphs are deposited on nutritionally-favourable leaves. The implications of the interleaf dispersal of apterous M. persicae for within- and between-plant spread of beet yellows virus (BYV) and beet mild yellowing virus (BMYV) are discussed.     

Alate production in an aphid in relation to ant tending and alarm pheromone

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate. 2. Ant‐tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal. 3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linné, 1758) ants. 4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae. 5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.     

蚜虫迁飞的研究进展

蚜虫的迁飞能造成危害扩展、病毒病传播和防碍人们的正常生活。蚜虫迁飞有其生理生态基础。寄主营养、蚜群拥挤度、天敌以及气候条件是刺激有翅蚜产生的主因素。蚜虫迁飞与卵巢发育存在明显的共轭关系。蚜虫迁飞多发生在晴朗的白天 ,并且温度、光照和风是影响迁飞行为的主导因子。蚜虫可上升到逆温层并随气流迁飞到上百公里以外的地方。目前 ,昆虫雷达观察、天气学分析和分子生物学方法已应用于蚜虫迁学的研究中 ,文章对蚜虫迁飞的生理生态基础、迁飞行为、影响迁飞的生态因子以及研究方法进行了综述 ,以期为蚜虫这类小型昆虫的迁飞研究提供指导     

Density-dependent dispersal may explain the mid-season crash in some aphid populations

Aphid population dynamics during the season show a characteristic pattern with rapid increase in numbers at the beginning followed by a sudden drop in the middle of the season. This pattern is usually associated with predation and/or change in food quality during the summer. By developing a mechanistic model of aphid population dynamics we show that this pattern can arise from density-dependent dispersal behaviour of aphids. The dynamics produced by the model were similar to those observed in real populations of the alder aphid (Pterocallis alni). The two mechanisms required for these oscillations to arise were the perception of density through the number of contacts with other individuals and the inter-generational transfer of information (the maternal effect). Both mechanisms are examples of delayed density-dependence and, therefore, this study adds to the evidence that delayed density-dependence might cause complex population dynamics. To reproduce the seasonal dynamics of the alder aphid with the model, the maternal effect was essential, indicating that this could be an important factor in alder aphid dynamics. According to our model, external regulations (e.g., predation and/or change in food quality) were not required to explain the highly oscillatory population dynamics of aphids during a season.     

Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting,settling and probing behaviour of its vector Aphis gossypii favouring its own spread

Plant pathogens are able to influence the behaviour and fitness of their vectors in such a way that changes in plant–pathogen–vector interactions can affect their transmission. Such influence can be direct or indirect, depending on whether it is mediated by the presence of the pathogen in the vector's body or by host changes as a consequence of pathogen infection. We report the effect that the persistently aphid‐transmitted Cucurbit aphid‐borne yellows virus (CABYV, Polerovirus) can induce on the alighting, settling and probing behaviour activities of its vector, the cotton aphid Aphis gossypii. Only minor direct changes on aphid feeding behaviour were observed when viruliferous aphids fed on non‐infected plants. However, the feeding behaviour of non‐viruliferous aphids was very different on CABYV‐infected than on non‐infected plants. Non‐viruliferous aphids spent longer time feeding from the phloem in CABYV‐infected plants compared to non‐infected plants, suggesting that CABYV indirectly manipulates aphid feeding behaviour through its shared host plant in order to favour viral acquisition. Viruliferous aphids showed a clear preference for non‐infected over CABYV‐infected plants at short and long time, while such behaviour was not observed for non‐viruliferous aphids. Overall, our results indicate that CABYV induces changes in its host plant that modifies aphid feeding behaviour in a way that virus acquisition from infected plants is enhanced. Once the aphids become viruliferous they prefer to settle on healthy plants, leading to optimise the transmission and spread of this phloem‐limited virus.     

Altered dispersal behaviour in parasitised aphids: parasitoid-mediated or pathology?

1. Several hypotheses concerning modified dispersal behaviour in aphids parasitised by aphidiine wasps (Hymenoptera: Braconidae: Aphidiinae) were tested in the laboratory. Behavioural changes may be host-mediated, parasitoid-mediated, or a by-product of trauma and pathology. 2. Mummification site varied with parasitoid species. Pea aphids (Acyrthosiphon pisum) parasitised by Aphidius ervi, Aphidius pisivorus, Monoctonus paulensis, and Praon pequodorum mummified near the aphids’ preferred feeding sites on bean plants, but those parasitised by Ephedrus californicus often died and mummified outside the colony, away from the plants. 3. Parasitism by E. californicus had a progressive effect on the behaviour of pea aphids. Approaching death, aphids lost motor control and frequently dropped off the host plant when disturbed. Dropped aphids were unable to return to the feeding site and mummified elsewhere. The proportion of aphids mummifying outside the colony increased with mummy density. 4. Mummification site was not influenced by the presence within the same colony of aphids parasitised by different species of aphidiine wasps. 5. The evidence does not support the hypothesis that mummification site selection in E. californicus is determined by a host- or a parasitoid-mediated change in aphid dispersal behaviour. Association-specific differences in the dynamics of larval development and growth between aphidiine species provide an equally valid and possibly more general explanation of mummification behaviour.     

Alarm pheromone mediates production of winged dispersal morphs in aphids

The aphid alarm pheromone ( E )- β -farnesene (EBF) is the major example of defence communication in the insect world. Released when aphids are attacked by predators such as ladybirds or lacewing larvae, aphid alarm pheromone causes behavioural reactions such as walking or dropping off the host plant. In this paper, we show that the exposure to alarm pheromone also induces aphids to give birth to winged dispersal morphs that leave their host plants. We first demonstrate that the alarm pheromone is the only volatile compound emitted from aphid colonies under predator attack and that emission is proportional to predator activity. We then show that artificial alarm pheromone induces groups of aphids but not single individuals to produce a higher proportion of winged morphs among their offspring. Furthermore, aphids react more strongly to the frequency of pheromone release than the amount of pheromone delivered. We suggest that EBF leads to a 'pseudo crowding' effect whereby alarm pheromone perception causes increased walking behaviour in aphids resulting in an increase in the number of physical contacts between individuals, similar to what happens when aphids are crowded. As many plants also produce EBF, our finding suggests that aphids could be manipulated by plants into leaving their hosts, but they also show that the context-dependence of EBF-induced wing formation may hinder such an exploitation of intraspecific signalling by plants.     

Observations on different methods of aphid trapping

Cylindrical and horizontal sticky traps painted in a range of spectral colours were used to determine the flight and landing behaviour of aphids. Data are also presented on aphid catches in suction traps at two heights and in light traps. Apart from colour sensitivity (yellow versus white) there was apparently a separate response to colour which in some species varied with season. Within yellow-sensitive species there was also a differential response to colour. With the experimental methods used, it was not possible to define mathematically the active and passive landing components on cylindrical traps. Though the active landing component was large it varied between aphid species. Most species caught on horizontal traps at ground level had been flying above 1 m. In some species the response of males to colour and their landing behaviour differed from that of viviparae and oviparae. Four years data from suction traps suggest that aphid species can be divided into three categories on the basis of the height at which they normally fly. One group, mostly tree-feeders, always show the greatest density at a high level (12.2 m) throughout the season. The second group always have the highest density at a low level (1 m) whilst a third group of species change at a specific date each autumn from a maximum density at 1–12.2 m. Attraction to light (moth trap) appeared to be linked with the grouping of species by height of flight. The interpretation of catch data is discussed in the light of these observations.     

Aerial distribution, flight behaviour and eggload: their inter-relationship during dispersal by the sweetpotato whitefly

1. The aerial distribution of Bemisia tabaci Gennadius (the sweetpotato whitefly) was studied during the early ascent phase of flight, to test the degree to which dispersal patterns reflect the flight behaviour of individuals.
2. Marked whiteflies were trapped at four heights between 0 and 7·2 m above fallow ground, and at six distances between 0 and 100 m from the insect source. Insects were trapped during a 2–3 h period after the initiation of flight activity during the summers of 1995 and 1996.
3. Analysis of trap catch data revealed a clear negative exponential relationship between height and aerial distribution, and a slightly weaker negative power relationship between distance and aerial distribution. Marked insects were caught in the uppermost traps adjacent to the source, indicating that a portion of the population had a strong capacity for ascent out of the flight boundary layer.
4. Eggload decreased with the height, but not the distance, at which whiteflies were trapped. Mean eggload close to the ground was significantly greater than that for those trapped at 4·8 and 7·2 m, supporting the hypothesis that there is a trade-off between flight and oogenesis in weak-flying insects.
5. Air temperatures during the trapping periods were positively correlated with the proportion of male and female B. tabaci caught in the highest traps, but not in the most distant traps.
6. The significance of these results for accurate prediction of whitefly dispersal is discussed, and the importance of individual's behaviour in determining dispersal patterns of small insects is emphasized.     

Ant semiochemicals limit apterous aphid dispersal

Some organisms can manipulate the nervous systems of others or alter their physiology in order to obtain benefit. Ants are known to limit alate aphid dispersal by physically removing wings and also through chemical manipulation of the alate developmental pathway. This results in reduced dispersal and higher local densities of aphids, which benefit ants in terms of increased honeydew and prey availability. Here, we show that the walking movement of mutualistic apterous aphids is also reduced by ant semiochemicals. Aphids walk slower and their dispersal from an unsuitable patch is hampered by ants. If aphid walking dispersal has evolved as a means of natural enemy escape, then ant chemicals may act as a signal indicating protection; hence, reduced dispersal could be adaptive for aphids. If, however, dispersal is primarily a means to reduce competition or to maintain persistent metapopulations, then manipulation by ants could be detrimental. Such manipulation strategies, common in host-parasite and predator-prey interactions, may be more common in mutualism than expected.     

The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour

1. The effects of predator species, aphid density, aphid age, diel period, and habitat complexity on the dropping behaviour of the pea aphid Acyrthosiphon pisum were assessed in a series of laboratory and field-cage experiments.
2. The presence of foliar-foraging predators significantly increased the proportion of aphids that dropped from alfalfa plants. In the absence of predators, less than 7% of the aphids dropped. Dropping more than doubled (14%) when one of three hemipteran predators , N. americoferus, G. punctipes or O. insidiosus , was present. Nearly 60% of the aphids dropped when the ladybird beetle, Coccinella septempunctata , was present.
3. Adult aphids showed a significantly higher propensity to drop than immature aphids, regardless of the presence or absence of predators. Aphid density had no effect on dropping behaviour.
4. Neither diel period nor habitat complexity had an effect on aphid dropping behaviour. Aphids were significantly more likely to drop in the presence of predators during either the day or night and from either early or late regrowth alfalfa.
5. A review of the factors affecting dropping behaviour, including those elucidated in this study, indicates that the propensity to drop from a plant is influenced by three factors: the risk of predation on the plant, the quality of the resource to be abandoned, and the risk of mortality in the new microhabitat.     

Dealing with food shortage: larval dispersal behaviour and survival on non‐prey food of the hoverfly Episyrphus balteatus

1. Predatory larvae often have to face food shortages during their development, and thus the ability to disperse and find new feeding sites is crucial for survival. However, the dispersal capacity of predatory larvae, the host finding cues employed, and their use of alternative food sources are largely unknown. These aspects of the foraging behaviour of the aphidophagous hoverfly (Episyrphus balteatus De Geer) larvae were investigated in the present study. 2. It was shown that these hoverfly larvae do not leave a plant as long as there are aphids available, but that dispersing larvae are able to find other aphid colonies in the field. Dispersing hoverfly larvae accumulated on large aphid colonies, but did not distinguish between different pea aphid race–plant species combinations. Large aphid colonies might be easier to detect because of intensified searching by hoverfly larvae following the encounter of aphid cues like honeydew that accumulate around large colonies. 3. It was further shown that non‐prey food, such as diluted honey or pollen, was insufficient for hoverfly larvae to gain weight, but prolonged the survival of the larvae compared with unfed individuals. As soon as larvae were switched back to an aphid diet, they rapidly gained weight and some pupated after a few days. Although pupation and adult hatching rates were strongly reduced compared with hoverflies continuously fed with aphids, the consumption of non‐prey food most probably increases the probability that hoverfly larvae find an aphid colony and complete their development.     

ON THE EVOLUTION OF DISPERSAL AND ALTRUISM IN APHIDS

How competitive interactions and population structure promote or inhibit cooperation in animal groups remains a key challenge in social evolution. In eusocial aphids, there is no single explanation for what predisposes some lineages of aphids to sociality, and not others. Because the assumption has been that most aphid species occur in essentially clonal groups, the roles of intra- and interspecific competition and population structure in aphid sociality have been given little consideration. Here, I used microsatellites to evaluate the patterns of variation in the clonal group structure of both social and nonsocial aphid species. Multiclonal groups are consistent features across sites and host plants, and all species—social or not—can be found in groups composed of large fractions of multiple clones, and even multiple species. Between-group dispersal in gall-forming aphids is ubiquitous, implying that factors acting ultimately to increase between-clone interactions and decrease within-group relatedness were present in aphids prior to the origins of sociality. By demonstrating that between-group dispersal is common in aphids, and thus interactions between clones are also common, these results suggest that understanding the ecological dynamics of dispersal and competition may offer unique insights into the evolutionary puzzle of sociality in aphids.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

Direct and Indirect Impacts of Infestation of Tomato Plant by Myzus persicae (Hemiptera: Aphididae) on Bemisia tabaci (Hemiptera: Aleyrodidae)

The impacts of infestation by the green peach aphid (Myzus persicae) on sweetpotato whitefly (Bemisia tabaci) settling on tomato were determined in seven separate experiments with whole plants and with detached leaves through manipulation of four factors: durations of aphid infestation, density of aphids, intervals between aphid removal after different durations of infestation and the time of whitefly release, and leaf positions on the plants. The results demonstrated that B. tabaci preferred to settle on the plant leaves that had not been infested by aphids when they had a choice. The plant leaves on which aphids were still present (direct effect) had fewer whiteflies than those previously infested by aphids (indirect effect). The whiteflies were able to settle on the plant which aphids had previously infested, and also could settle on leaves with aphids if no uninfested plants were available. Tests of direct factors revealed that duration of aphid infestation had a stronger effect on whitefly landing preference than aphid density; whitefly preference was the least when 20 aphids fed on the leaves for 72 h. Tests of indirect effects revealed that the major factor that affected whitefly preference for a host plant was the interval between the time of aphid removal after infestation and the time of whitefly release. The importance of the four factors that affected the induced plant defense against whiteflies can be arranged in the following order: time intervals between aphid removal and whitefly release > durations of aphid infestation > density of aphids > leaf positions on the plants. In conclusion, the density of aphid infestation and time for which they were feeding influenced the production of induced compounds by tomatoes, the whitefly responses to the plants, and reduced interspecific competition.     

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.     

Oviposition behaviour of the aphid parasitoid,Aphidius ervi: Are wet aphids recognized as host?

Females of the central European population of the aphid parasitoid, Aphidius ervi, did not attack wet pea aphids (Acyrthosiphon pisum) that were washed previously with water. After 1 hour, this phenomenon disappeared and A. ervi attacked washed hosts to the same degree as dry ones. Similarly, A. ervi attacked dead aphids killed in liquid nitrogen readily if they were dry but not if they were wet. This effect was also reversible and disappeared after 1 h. When A. ervi females were foraging on broad beans (Vicia faba), they laid significantly more eggs into dry aphids than into wet aphids. Resource utilization of wet aphids, however, was significantly lower in this design than in Petri dishes, due to a changed drop-off behaviour of the aphid. We conclude that females did not use visual cues for host recognition but instead relied on chemical cues. These cues may be covered by a thin water layer directly after aphids became wet. Our results also demonstrate the importance of abiotic factors for the estimation of the reproductive success of parasitoids in the field.     

Low propensity for aerial dispersal in specialist spiders from fragmented landscapes

Aerial dispersal by ballooning is a passive flight, by which wind drag generates an upward lift on a silk thread. It is likely to reflect an aerial lottery, in which the absence of flight direction control is a serious cost for long-distance dispersal in a fragmented landscape. For species occurring in one patchily distributed habitat type, dispersal should evolve in a different way from morphological traits, directly linked to active dispersal. Therefore, we expect that if the risk of landing in an unsuitable habitat is lower than the probability of reaching a suitable habitat, selection should benefit a well-developed ballooning behaviour. We investigated interspecific variation in the ballooning-initiating tiptoe behaviour as it is linked to spider dispersal performance. Our results indeed indicate that ballooning performance is negatively related to habitat specialization in spiders from patchy grey dunes, so habitat specialists are characterized by poorly developed dispersal behaviour. These findings are concordant with recent insights that dispersal is selected as risk spreading in generalists, while it is selected against in specialist species.