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Keywords:

  • Aphid;
  • emigration;
  • fecundity;
  • mid-season population crash;
  • mortality;
  • natural enemies;
  • plant quality;
  • weather

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References

Abstract.  1. Aphid populations on agricultural crops in temperature regions collapse over a few days from peak numbers to local extinction soon after mid-summer (e.g. mid-July in the U.K.). The populations recover 6–8 weeks later. There is anecdotal or incidental evidence of an equivalent mid-season population crash of aphids on grasses and forbs in natural vegetation.

2. The ecological factors causing the mid-season population crash of aphids include a decline in plant nutritional quality and increased natural enemy pressure as the season progresses. Extreme weather events, e.g. severe rainstorms, can precipitate the crash but weather conditions are not a consistent contributory factor.

3. The population processes underlying the crash comprise enhanced emigration, especially by alate (winged) aphids, depressed performance resulting in reduced birth rates, and elevated mortality caused by natural enemies.

4. Mathematical models, previously applied to aphid populations on agricultural crops, have great potential for studies of aphid dynamics in natural vegetation. In particular, they can help identify the contribution of various ecological factors to the timing of the population crash and offer explanations for how slow changes in population processes can result in a rapid collapse of aphid populations.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References

Aphids have an immense capacity for population increase. Populations of the summer morphs, which are parthenogenetic and viviparous, can double in just 3 days, such that a single aphid weighing 1 mg can, in just 6 months, theoretically generate a population of total weight more than 100 times the global human population (assuming 6 billion people of mean weight 50 kg). The fact that summer aphid infestations do not multiply to this extent is a consequence of a number of biological and abiotic constraints on aphid population increase. Identifying the factors that control aphid populations is a central topic in aphid ecology.

Most research on aphid population dynamics has been conducted on tree-dwelling aphids (Dixon, 1998). These aphids are relatively easy to study because individual trees persist over many years, facilitating long-term analysis. In the summer months, the nutritional quality of the phloem sap of trees is generally very low (Douglas, 1993, 2003). Presumably as an evolutionary response to this seasonally predictable shift in tree phloem nutrients, various tree-dwelling aphid species exhibit a period of programmed cessation of development and reproduction, such that populations persist as a single developmental stage (adult or larval, varying among species) for some weeks (e.g. Dixon, 1975; Kawada, 1988). This condition, which appears to be programmed, is known as aestivation in the aphid literature (Dixon, 1998).

In the summer months, the phloem sap of grasses and forbs is generally accepted to be more nutritious for aphids than that of trees (Kennedy & Booth, 1951; Mackenzie & Dixon, 1990; Douglas, 1993). Consistent with this, aphid populations on grasses and forbs do not display aestivation and their dynamics are expected to be very different from those of tree-dwelling aphids. Most investigations have been conducted by agricultural entomologists, with a primary aim to predict the timing and magnitude of peak aphid populations on arable crops. Many of these agricultural studies in temperate regions have revealed a rapid decline from peak aphid numbers, usually over 3–7 days, sometime after midsummer (e.g. mid-July in the U.K. Fig. 1), leaving plants essentially aphid-free. Aphids are not found on other plants in the locality and populations tend to recover no earlier than 6–8 weeks after their disappearance (Fig. 1b). The dramatic decline in aphid numbers is termed the mid-season population crash, and it has been described for a variety of aphid species on cereal and broad-leaved crops, as surveyed in Table 1.

image

Figure 1. Numbers during the summer months of (a) Macrosiphum euphorbiae and Myzus persicae (data from Parker et al., 2000) and (b) Myzus persicae (redrawn from Fig. 3 of MacKauer & Way, 1976), in the absence of chemical control.

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Table 1.  Causal ecological factors and aphid population processes inferred to contribute to the mid-season crash in aphid populations on agricultural crops.
Aphid speciesCrop speciesEcological factor (why crash?)Population process (how crash?)Reference
On cereal crops
Diuraphis noxiaHordeum vulgareHigh temperaturesMortalityBasky (1993)
 Avena sativa Emigration 
Diuraphis noxiaTriticum durumNatural enemiesMortalityHopper et al. (1995)
  Plant quality  
Metopolophium dirhodumTriticum durumPlant qualityAlate emigration linked to high aphid densityHoward & Dixon (1992)
Metopolophium dirhodum & Sitobion avenaeTriticum durumPlant qualityReduced aphid fecundityWatt (1979)
Metopolophium dirhodum & Sitobion avenaeHordeum vulgare Triticum durumNatural enemies Plant qualityMortality EmigrationJones (1979)
Rhopalosiphum padi, Rhopalosiphum maidis Sitobion avenaeHordeum vulgare Triticum durum Avena sativaPlant quality RainstormsAlate production MortalityBa-Angood & Stewart (1980)
Sitobion avenaeTriticum durumPlant qualityEmigration linked to high aphid densityWatt & Dixon (1981)
On broad-leaved crops
Acyrthosiphon pisumPisum sativa Alate emigration linked to high aphid densityMcVean et al. (1999)
Macrosiphum euphorbiae, Myzus persicae & Aphis nasturtiiSolanum tubersosumNatural enemies Boiteau (1986)
Macrosiphum euphorbiae, Myzus persicae, Aulocorthum solani & Aphis gossypiiSolanum tuberosumNatural enemies Weather Nakata (1995a,b)
Macrosiphum euphorbiae & Myzus persicaeSolanum tuberosumPlant quality Natural enemiesDecreased fecundity Increased mortality EmigrationKarley et al. (2002, 2003)
Myzus persicaeSolanum tuberosum Beta vulgarisPlant quality Natural enemiesReduced fecundity MortalityMackauer & Way (1976)
Myzus persicaeBeta vulgarisPlant qualityIncreased mortalityKift et al. (1998)

Various publications on the ecology of aphid populations on grasses and forbs in natural vegetation include datasets indicative of rapid population declines in the mid-summer; Müller et al. (1999) and Weisser (2000) are recent examples. Although the studies on aphids in natural vegetation are generally less systematic than those on crops, especially in relation to the ecological factors triggering the crash, they indicate that the disappearance of aphids from agricultural crops in the summer is not restricted to the simplified ecosystems of arable crops or caused by specific agricultural practices, such as harvesting of the crops or spraying with agricultural pesticides. In other words, the mid-season population crash may be a widespread and possibly a general feature of aphid populations on forbs and grasses in temperate regions.

The purpose of this review article is to increase the awareness among ecologists studying insect populations in natural vegetation of the existence of the mid-season population crash with examples from the relevant agricultural literature. The article is structured to address the two core questions posed by the crash. First, why do aphid populations crash, i.e. what ecological factors cause the crash? Second, how do they crash, i.e. how important are each of the classical population processes of birth, death, and migration in mediating the crash?

Why do aphid populations crash?

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References

Three broad ecological factors have been reported to cause aphid population crashes on agricultural crops: weather conditions, increased natural enemy pressure, and a decline in plant quality (Table 1). These three factors are now considered in turn.

Severe weather events, especially intense rainstorms and strong winds, have been found to decimate or eliminate aphid populations on crops (e.g. Jones, 1979; Ba-Angood & Stewart, 1980), but such exceptional events do not account for the population crash in consecutive years and at multiple locations (Parker et al., 2000). Extreme temperatures have been demonstrated repeatedly to depress aphid performance (e.g. Asin & Pons, 2001; Morgan et al., 2001), and high summer temperatures have been linked to the timing of the mid-season crash for both Macrosiphum euphorbiae (Barlow, 1962) and Diuraphis noxia (Basky, 1993). However, other studies have revealed no apparent relationship between temperature, or any other weather variable, and the timing of the population crash (e.g. Karley et al., 2003). The crash generally occurs a few weeks after midsummer, raising the possibility that the shift from increasing to decreasing day-length (from the days before to the days after the midsummer maximum) may influence the aphid populations. This remains to be investigated. A possible precedent for a role of day-length in aphid population processes is the important role of short day-length (or long night-length) as a trigger for the production of sexual morphs of aphids (Kawada, 1988).

Natural enemy attack can severely depress aphid numbers: aphids are consumed, parasitised, or infected by a range of specialist and generalist natural enemies, including syrphid and chrysopid larvae, coccinellids, carabids, spiders, hymenopteran parasitoids, and entomophagous fungi (Kidd & Jervis, 1995). The variety and abundance of natural enemies vary with crop species, management regime, and season (Boiteau, 1986; Nakata, 1995b; Losey & Denno, 1999; French et al., 2001), but generally the numbers tend to increase and reach a maximum within days of the aphid population peak (Mackauer & Way, 1976; Karley et al., 2003). Short-term or partial natural enemy exclusion experiments confirm that aphid populations are depressed by natural enemies, for example by 10–70% on potato crops (Boiteau, 1986; Karley et al., 2003) and by 30–100% on cereal crops (Jones, 1979; Holland & Thomas, 1997; Sigsgaard, 2002). The variation in impact of natural enemies on aphid populations is unsurprising because natural enemy assemblages vary widely in composition and activity, with potentially complex interactions among natural enemies through intraguild predation (Rosenheim, 1998) and synergistic interactions (e.g. Losey & Denno, 1999). However, one crucial experiment remains to be conducted: to establish whether complete exclusion of natural enemies throughout the period of summer population development prevents the mid-season population crash of aphids.

The second key biotic factor that may influence the mid-season population crash of aphids is plant suitability. The behaviour and performance of aphids are known to vary with plant developmental age and growth conditions, including nutrient and water availability and temperature, attributable to variation in plant primary nutrients and secondary metabolites (reviewed in Douglas, 2003). However, research to prove that plant quality, in terms of phloem nutrient or allelochemical composition, declines in parallel with changes in aphid performance and the population crash is sparse. To our knowledge, it has been explored only in potato crops, which show a shift in phloem amino acid composition from a glutamine-dominated profile to a glutamate-dominated profile in the weeks immediately preceding the mid-season aphid population crash (Karley et al., 2002, 2003). When reared on artificial diets of composition based on these two phloem profiles, the potato aphids Myzus persicae and Macrosiphum euphorbiae performed better on diets mimicking the younger plants with the glutamine-dominated profile (Karley et al., 2002). However, the difference in performance of aphids on the two diet compositions, although statistically significant, was not very substantial, suggesting that the identified differences in nutrients alone were not sufficient to account for the population crash.

In summary, although abiotic factors, natural enemies and plant suitability have all been implicated as determinants of the mid-season population crash of aphid populations, none has been shown definitively to be the sole factor causing the rapid decline in aphid populations. In many situations, the aphid population crash, like other aspects of the population dynamics of phytophagous insects, is probably caused by complex interactions among these factors. To illustrate, the performance of aphids and their natural enemies might be differentially affected by temperature (Skirvin et al., 1997); plant nutrient content and allocation to defence is strongly influenced by abiotic factors including temperature, rainfall, and wind speed (Bernays & Chapman, 1994); and susceptibility to natural enemies may be enhanced by induced responses of the plant to aphid infestation (van der Putten et al., 2001).

A further biotic factor that has not, to date, been considered in discussions of the causes of the mid-season population crash of aphids is the microbiology of the insects. Virtually all aphids bear symbiotic bacteria of the genus Buchnera, on which they are absolutely dependent, and one-to-several other types, known as secondary bacteria. Although the secondary bacteria are not required by the insect, they can influence aphid performance on certain plants (Chen et al., 2000), susceptibility to parasitoids (Oliver et al., 2003), and tolerance of elevated temperature (Montllor et al., 2002). It remains to be established whether the prevalence of secondary bacteria in aphid populations or the abundance of secondary bacteria in individual aphids changes during the season and, thereby, affects the timing or scale of the mid-season crash by altering aphid responses to changes in plant quality, natural enemy abundance, and abiotic factors.

How do aphid populations crash?

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References

Emigration, depressed birth rates and elevated death rates can, in principle, contribute to a decline in aphid numbers in one locality.

All life stages and morphs of aphids can emigrate from plants by dropping or walking from the plant. Adult alates (the winged morph) can additionally fly away. A number of aphid species, known as holocyclic species, display a relatively synchronised disappearance from primary (winter) hosts in early spring, mediated by the production of alates that migrate to secondary (summer) hosts; this is followed some months later by an autumn migration of sexual forms back to the winter host. There is, however, no consistent evidence that the mid-season crash is correlated with a wave of asexual alate production and emigration from plants in the summer. Increased numbers of alates on the plants and recovered in suction traps have been reported at the time of the aphid population peak in some studies of aphids on cereal crops (e.g. Ba-Angood & Stewart, 1980; Watt & Dixon, 1981; Howard & Dixon, 1990) and pea crops (Bommarco & Ekbom, 1996; McVean et al., 1999), but other studies have identified very few alates in peak aphid populations on cereals (Hopper et al., 1995), potatoes (Nakata, 1995a; Karley et al., 2003), and sugar beet (Williams et al., 1999). One study has additionally revealed an increase in the incidence of aphids dropping from plants at the time of the mid-season population crash, but the contribution of this process to the overall population decline was probably small (Karley et al., 2003).

Evidence for the contribution of depressed birth rates and increased mortality to the mid-season population crash is correspondingly patchy. While plant maturation undoubtedly affects aphid performance and fecundity (Table 1), there is no evidence to implicate a programmed cessation of reproduction. This is in sharp contrast to various tree-dwelling aphids, which display an extended pre-reproductive period and absence of larval aphids from the population for several weeks during the summer (Dixon, 1998), linked to an uncoupling of maternal growth and development from that of the embryos (Douglas, 2000). Additionally, there is no evidence for sudden mass mortality of aphids in crops at the time of the population crash.

These data suggest that the very rapid mid-season population crash can be caused by slow-acting, non-catastrophic processes: depressed birth rates, attributable to low plant quality on aphid fecundity, and enhanced mortality associated with heightened natural enemy activity. Although this conclusion appears counter-intuitive, mathematical modelling of the processes underlying the population crash indicates that the combined effects of these slow-acting processes can be sufficient to cause a sudden population crash (Karley et al., 2003).

We anticipate that the relative importance of these processes (i.e. depressed birth rates and increased death rates) and emigration will be found to vary with plant and aphid species and environmental circumstance.

Future perspectives

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References

The title of this article is a question, not a statement. The available data are insufficient to reach any definitive conclusions as to why or how the mid-season crash of aphid populations occurs on agricultural crops, but they do suggest strongly that multiple factors and processes are involved and that relatively slow changes in population processes over the season might precipitate the rapid crash in aphid numbers by mid-summer. A key priority is to establish the relative importance of the candidate mechanisms among different aphid–plant combinations, between years and with location, and the possibly complex interactions among the different processes.

Understanding the mechanism of the population crash is a major challenge. In many studies, the link between the ecological factors driving population change and the underlying population processes is largely speculative. Mathematical modelling techniques offer a powerful tool to investigate the interplay among different ecological factors and population processes shaping the mid-season population crash. To date, most population models have concentrated principally on identifying the climatic variables which predict the timing and magnitude of the summer population peak, e.g. deviations from mean winter temperature (Parker, 1997), or linear combinations of minimum, mean, and maximum monthly temperatures across several months (Thacker et al., 1997; Parker, 1998;). These approaches and refinements, especially the use of degree-days (e.g. Ro et al., 1998), use relatively simple linear statistical techniques which must necessarily have limitations in predicting complex, nonlinear phenomena. These approaches also lack any underlying mechanism, which is a severe limitation in extending such models to include additional parameters.

Alternative, nonlinear, modelling approaches are available. One example is the approach of Ekbom et al. (1992), who coupled stochastic individual-based predator foraging simulations with a temperature-driven phenological model of aphid growth. These authors demonstrate that predation can induce a crash, or prevent a peak, in Rhopalosiphum padi populations, but only if this predation is of sufficient magnitude and occurs at the same time or soon after the aphids colonise the crop. A different approach based on the excitable medium paradigm has been applied recently to simulate the mid-summer population crash in Macrosiphum euphorbiae on potato crops (Karley et al., 2003). Detailed individual-based data for the abundance and behaviour of natural enemies for plant developmental effects on aphid performance were used to develop a population-based model, with parametrically forced differential equations. This revealed that the rapid change in population numbers could result from small, incremental changes in ecological factors, specifically seasonal changes in plant nutritional quality and natural enemy abundance. The model also explained the observed inter-annual differences in aphid population dynamics.

Individual-based quantification and modelling of aphid population processes, as outlined above, certainly represent an advance in our understanding of the mid-season population crash, but there is a very real opportunity for further developments in modelling approaches. Most models used to explore aphid population dynamics, including the population crash, are spatially homogeneous (Parker, 1997; Thacker et al., 1997; Ro et al., 1998; Karley et al., 2003) or allow limited heterogeneity at the level of a row of plants before averaging (Ekbom et al., 1992). These may be inadequate, especially in systems where emigration of alates plays an important role in the population crash. Greater modelling attention deserves to be given to spatial processes; but this, in turn, requires further empirical data and modelling resources.

We envisage that further advance in understanding of the mid-season population crash will be achieved by coupling these modelling approaches with experimental investigation of the interactions between ecological factors and population processes. In relation to agricultural pests, a full understanding of the ecological causes and population processes underlying the population crash should lead to identification of management practices that either are tailored to suit the actual or anticipated risk of aphid damage (e.g. Parker et al., 2002) or advance the onset of the crash, so reducing the duration and abundance of aphid infestations of crops. More widely, the significance of the mid-season population crash to the dynamics of aphid populations on forbs and grasses in ‘natural’ vegetation deserves greater consideration. For example the timing and scale of the population crash may influence the number of sexual aphids produced in the autumn, which is an important determinant of spring populations of certain aphid species (e.g. Way et al., 1981).

The mid-season population crash also has implications for the abundance and distribution of other taxa influenced by aphid infestations, including the plants on which the aphids feed, other phytophages with which they may compete, and their natural enemies. These issues may be particularly important for the structuring of non-agricultural terrestrial communities in which aphids are seasonally important. Research on aphid populations on forbs and grasses in natural vegetation may reveal the mid-season population crash as a vital element in the population dynamics of aphids and other species in terrestrial communities in the summer months.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Why do aphid populations crash?
  5. How do aphid populations crash?
  6. Future perspectives
  7. References
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