Not all aphids get eaten – “bottom-up” wins this time

In the lecture that I introduce aphids to our entomology MSc students I show them two quotes that illustrate the prodigious reproductive potential of these fantastic animals.

“In a season the potential descendants of one female aphid contain more substance than 500 million stout men “– Thomas Henry Huxley (1858) and “In a year aphids could form a layer 149 km deep over the surface of the earth.  Thank God for limited resources and natural enemies” – Richard Harrington (1994).

I was a little discomfited whilst researching this article to find that both Huxley and I had been short-changed, although the original quote does hint at the mortality factors that an aphid clone faces during its life.

The original words and the morphed ‘quote’

 

Both these quotes acknowledge the contribution that both bottom-up and top-down factors have on aphid populations.  For those not familiar with the ecological jargon, ecologists have at times over the last 40 years or so, got quite territorial* about whether herbivorous insect populations are regulated by top-down e.g. predators or bottom-up e.g. host plant quality, factors (e.g. Hunter & Price, 1992).  Who is in charge of an aphid clone’s destiny, natural enemies or the food plant?

Aphids are the favourite food of several insect species; ladybirds (but not all species), lacewing larvae, hoverfly larvae, and also the larvae of some Cecidomyiid flies (Aphidoletes spp.), and Chamaemyiid flies (e.g. Leucopis glyphinivora).  They are also attacked by other Hemipteran species, such as Anthocoris nemorum.   Those insects that make a living almost solely from aphids, are termed aphidophagous and every three years you can, if you feel like it, attend an international conference devoted to the subject 🙂

As well as these specialist predators, aphids are also preyed upon by more generalist predators, such as carabid and staphylinid beetles, harvestmen and spiders. Aphids also provide a nutritious snack for birds and bats.  Faced with all these hungry and voracious predators you might wonder why it is that aphids ever get numerous enough to become pests.  There are two answers, their fantastic reproductive rates and second, aphids, despite appearing soft and squishy, do have anti-predator defence mechanisms.  These range from kicking predators in the face, dropping off the plant, gumming up the jaws of predators by smearing them with wax from their siphunculi, and even jumping out of the way of the predator (Dixon, 1958).  On top of all that,  many are extremely unpalatable and even poisonous.

Some population modelling work from the 1970s explains why aphids can often become pests, as well as introducing us to the concept of population dynamics geography; the endemic and epidemic ridges, and my favourite, the natural enemy ravine (Southwood & Comins, 1976).

The geography of population dynamics from Southwood & Comins (1976)

 

They suggested that if enough predators are already present in the habitat or arrive shortly after the aphids, then the aphid population either goes extinct or only reaches the “endemic ridge”.  The phenomenal rate at which aphids can reproduce under favourable conditions, usually gets them past the “natural enemy ravine” and up into “epidemic ridge” with only a slight slowdown in population growth.   Evidence for the “natural enemy ravine” is not very convincing and I feel that the suggestion that the dip in population growth at the start of the season is due to intermittent immigration by winged aphids and not the action of polyphagous predators (Carter & Dixon, 1981) is pretty convincing.   That said, later modelling work suggested that the subsequent growth of aphid populations could be slowed down by the action of natural enemies Carter et al., 1982).

Aphids, despite their ability to produce baby aphids extremely quickly, are not equally abundant all year round. Those of us who want to collect aphids know that the best time of year is early in the season, spring and early summer.  This is the time when the plant sap is flowing quickly and is rich in nutrients, especially nitrogen, which aphids need in large quantities.    A characteristic of aphid populations is the way they suddenly disappear during July, a phenomenon known as the “mid-summer or mid-season crash”.  This is not just a phenomenon confined to aphids living on ephemeral herbaceous hosts, it happens to tree-dwelling aphids too e.g. the sycamore aphid, Drepanoisphum platanoidis.  At Silwood Park, where I monitored sycamore aphid populations on fifty-two trees for twenty years**, I saw the same pattern of a rapid build-up followed by an equally rapid collapse every year.  The pattern was the same in both high population and low population years and happened at pretty much the same time every year.  Herbivorous insects are, as you might expect, strongly

High and low population years of sycamore aphid, Drepanosiphum platanoidis at Silwood Park

affected by the quality of their host plant, the availability of nitrogen in the leaves being of most importance (Awmack & Leather, 2002).  Aphids are no exception, and their whole-life cycle is adapted to the ever-changing, but predictable availability of soluble nitrogen and water in their host plants (Dixon, 1977).  Plants become less suitable for aphids as their tissues mature and they lock their nitrogen away in the leaves and other structures, rather than transporting it around in the phloem as they do in spring and autumn (Dixon, 1976).

Aphids respond in two ways to a decline in the nutritional quality of their host plant, they reduce the number of offspring they produce (e.g. Watt, 1979) and those offspring they produce are winged (e.g. Parry, 1977), or if already winged, more likely to take flight and seek new better quality host plants (e.g. Dixon, 1969; Jarosik & Dixon, 1999).  In some aphids there is also an increase in intrinsic mortality (e.g. Kift et al., 1998).

The mid-season crash is not confined to abundant and common aphids, rare aphids show exactly the same changes in their populations, and this is similarly attributed to changes in the nutritional quality of the aphid host plant leading to increased dispersal (e.g. Kean, 2002).

Population crash of the rare aphid Paradoxaphis plagianthi in New Zealand (data from Kean, 2002).

Although some authors, notably Alison Karley and colleagues have suggested that it is the action of natural enemies and not host nutrition that drives the mid-season crash (Karley et al., 2003, 2004), the overwhelming evidence points to the production of winged (alate) morphs and their dispersal, being the major factor in causing the mid-season crash as the graphs below illustrate.

Cereal aphids on wheat showing increased alate production coinciding and subsequent population crash on cereal crops. Data from Wratten, 1975).

Green spruce aphid, Elatobium abietinum on Norway spruce at Silwood Park, showing the population crash and associated increase in the number of winged aphids. Data from Leather & Owuor (1996).

Green spruce aphid in Ireland, population crash associated with marked decline in fecundity and production of winged forms. Data from Day (1984)

Data presented by Way & Banks (1968) might lend some support to the idea that natural enemies cause the mid-season crash.  A close examination of the data however, which might at first glance suggest that keeping natural enemies away, allows aphid populations to prosper, reveals that the process of excluding natural enemies also prevents the dispersal of the winged aphids, which have no choice but to stay on the host plant and reproduce there.

Aphis fabae populations on Spindle bushes from Way & Banks (1968). Top line shows the population kept free of predators until August 2^nd, bottom line, exposed to predators.

Moreover, as the authors themselves state “the rise to peak density in each year, coincided with an enormous increase in the proportion of individuals destined to become alatae” (Way & Banks, 1968).   I do not dispute that natural enemies have an effect on aphid populations, but in my opinion, the evidence does not support the hypothesis that they are the driving force behind the mid-season crash.  Rather, the major factor is the reduction in host quality, caused by a decline in the nutritional status of the plant and overcrowding of the aphids, leading to reduced fecundity and an increase in winged dispersers.

I don’t deny that the natural enemies do a very good mopping-up job of those aphids that are left behind, but they are not the force majeure by any stretch of the imagination. Most aphids do not get eaten 🙂

 

References

Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817-844.

Carter, N. & Dixon, A.F.G. (1981) The natural enemy ravine in cereal aphid population dynamics: a consequence of predator activity or aphid biology? Journal of Animal Ecology, 50, 605-611.

Carter, N., Gardner, S.M., Fraser, A.M., & Adams, T.H.L. (1982) The role of natural enemies in cereal aphid population dynamics. Annals of Applied Biology, 101, 190-195.

Day, K.R. (1984) The growth and decline of a population of the spruce aphid Elatobium abietinum during a three  study, and the changing pattern of fecundity, recruitment and alary polymorphism in a Northern Ireland Forest. Oecologia, 64, 118-124.

Dixon, A.F.G. (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London, 110, 319-334.

Dixon, A.F.G. (1969) Population dynamics of the sycamore aphid Drepanosiphum platanoides (Schr) (Hemiptera: Aphididae); migratory and trivial flight activity. Journal of Animal Ecology, 38, 585-606.

Dixon, A.F.G. (1976) Factors determining the distribution of sycamore aphids on sycamore leaves during summer. Ecological Entomology, 1, 275-278.

Dixon, A.F.G. (1977) Aphid Ecology: Life cycles, polymorphism, and population regulation. Annual Review of Ecology & Systematics, 8, 329-353.

Harrington, R. (1994) Aphid layer. Antenna, 18, 50-51.

Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders – heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73, 724-732.

Huxley, T.H. (1858) On the agmaic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society London, 22, 193-219.

Jarosik, V. & Dixon, A.F.G. (1999) Population dynamics of a tree-dwelling aphid: regulation and density-independent processes. Journal of Animal Ecology, 68, 726-732.

Karley, A.J., Parker, W.E., Pitchford, J.W., & Douglas, A.E. (2004) The mid-season crash in aphid populations: why and how does it occur? Ecological Entomology, 29, 383-388.

Karley, A.J., Pitchford, J.W., Douglas, A.E., Parker, W.E., & Howard, J.J. (2003) The causes and processes of the mid-summer population crash of the potato aphids Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research, 93, 425-437.

Kean, J.M. (2002) Population patterns of Paradoxaphis plagianthi, a rare New Zealand aphid. New Zealand Journal of Ecology, 26, 171-176.

Kift, N.B., Dewar, A.M. & Dixon, A.F.G. (1998) Onset of a decline in the quality of sugar beet as a host for the aphid Myzus persicae.  Entomologia experimentalis et applicata, 88, 155-161.

Leather, S.R. & Owuor, A. (1996) The influence of natural enemies and migration on spring populations of the green spruce aphid, Elatobium abietinum Walker (Hom., Aphididae). Journal of Applied Entomology, 120, 529-536.

Parry, W.H. (1977) The effects of nutrition and density on the production of alate Elatobium abietinum on Sitka spruce. Oecologia, 30, 637-675.

Southwood, T.R.E. & Comins, H.N. (1976) A synoptic population model.  Journal of Animal Ecology, 45, 949-965.

Watt, A.D. (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolphium dirhodum. Annals of Applied Biology, 91, 147-157.

Way, M.J. & Banks, C.J. (1968) Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter host Euonymus europaeus L. Annals of Applied Biology, 62, 177-197.

Wratten, S.D. (1975) The nature of the effects of the aphids Sitobion avenae and Metopolophium dirhodum on the growth of wheat. Annals of Applied Biology, 79, 27-34.

 

Post script

For those interested this is how Huxley arrived at his number of potential descendants, and here I quote from his paper,  “In his Lectures, Prof. Owen adopts the calculations taken from Morren (as acknowledged by him) from Tougard that a single impregnated ovum  of Aphis may give rise, without fecundation, to a quintillion of Aphides.” I have not, so far, been able to track down Tougard.

Morren, C.F.A. (1836) sur le Puceron du Pecher, Annales des Sciences Naturelle series 2. vi.

You may not know what a grain is, so to help you visualise it, 7000 grains equals a pound so 2 000 000 grains gives you 286 pounds, or 20 stone or approximately 130 Kg depending on where you come from J

 

*and generated some magnificent paper titles and quite acrimonious responses J Hassell, M.P., Crawley, M.J., Godfray, H.C.J., & Lawton, J.H. (1998) Top-down versus bottom-up and the Ruritanian bean bug. Proceedings of the National Academy of Sciences USA, 95, 10661-10664.

**A true labour of love as I also counted maple aphids, orange ladybirds, winter moth larvae and any of their predators and parasites that I came across J

 

Not all aphids get lost

Although aphids are very good at kicking, we know that aphids would not be very good at football as they are very short-sighted (Doring et al., 2008) but does that mean that they are not very good at finding their host plants? There is a common misperception, and not just confined to non-entomologists, that aphids are no more than aerial plankton. In 1924 Charles Elton

whilst on an expedition to Nordaustlandet* (the second largest of the Spitsbergen group and almost entirely covered by ice) reported finding large numbers of aphids, many still alive, later identified as Dilachnus piceae (now known as Cinara piceae) (Elton, 1925).

Cinara piceae the Greater Black Spruce Aphid –big and beautiful.

 

He suggested that the aphids came from the Kola Peninsula, a distance of about 800 miles (almost 1300 km) due to the strong south and south-east winds blowing at the time. He estimated that they would have made the journey within twelve to twenty-four hours. This was regarded as being an example of totally passive migration and used as one of many examples of aerial plankton** (Gislen, 1948). This is, however, probably not giving aphids credit for what they are capable of doing when it comes to flight. Berry & Taylor (1968), who sampled aphids at 610 m above the grounds using aeroplanes, implied that the aphids, although using jet streams, were flying rather than floating (page 718 and page 720) and that they would descend to the ground in the evening and not fly during the night.

Aphids don’t usually fly during the night. (From Berry & Taylor (1968)).

Dixon (1971) interprets this somewhat differently and suggests that the “movement of the air in which it is flying determines the direction of its flight and the distance it will travel” but then goes on to say “after flying for an hour or two aphids settle indiscriminately on plants”. So yes the speed of the air in which the aphid is flying will determine how far it flies in a set time, but as aphids can fly much longer than an hour or two, active flights of from between 7-12 hours have been recorded (Cockbain, 1961), this rather suggests that the aphids are making a “decision” to stop flying and descend from the jet stream. That said, in the words of the great C.G. Johnson “aphids are weak flyers”, they cannot make progress against headwinds of more than 2 km per hour (Johnson, 1954), although Trevor Lewis gives them slightly more power and suggests that the can navigate against winds of up to 3 km per hour (Lewis, 1964).

Whatever the upper limit is, it doesn’t mean that they are powerless when it comes to ‘deciding’ when to stop flying. In the words of Hugh Loxdale and colleagues, “aphids are not passive objects” (Loxdale et al, 1993). Aphidologists, were until the 1980s (Kennedy, 1986), generally somewhat sceptical about the ability of aphids to direct their flight in relation to specific host finding from the air and not just flying towards plants of the right colour (Kennedy et al., 1961), or at all after take-off (Haine, 1955). The general consensus now, is that aphids control the direction of their flight in the boundary layer*** but that it is determined by the wind at higher altitudes (Loxdale et al., 1993).   Whilst we are discussing viewpoints, another point of debate is on whether aphids migrate or not. Loxdale et al., (1993) state that “migration can be viewed ecologically as population redistribution through movement, regardless of whether deliberate of uncontrolled or from the behavioural viewpoint of a persistent straightened-out movement affected by the animal’s own locomotory exertions or by its active embarkation on a vehicle”. In the case of aphids the vehicle could be the wind. Under both definitions, aphids can be defined as undertaking migrations. Long-distance migration by aphids is defined as being greater than 20 km and short-distance (local) migration being less than this (Loxdale et al., 1993). Long-distance migration is likely to be the exception rather than the rule with most aphids making local flights and not venturing out of the boundary layer, sometimes travelling distances no more than a few hundred metres (Loxdale et al., 1993).

There are different types of winged aphids (morphs) and these show different angles of take-off and rates of climb.  In Aphis fabae for example, which host –alternates between spindle and bean, the gynoparae which migrate from the secondary host to the primary host, have a steeper angle of take-off and climb more rapidly than the alate exules which only disperse between the secondary host plants (David & Hardie, 1988).

http://influentialpoints.com/Images/Rhopalosiphum_padi_emigrant_alate_departing_from_primary_host_c2013-05-21_11-25-12ew.jpg

The gynoparae are thus much more likely to end up in the jet stream and be carried longer distances, with, of course, a greater chance of getting lost (Ward et al., 1998). The alate exules however, may only land in the next field or even in the same one, and easily find a new host plant (Loxdale et al., 1993). These differences between the morphs of host alternating aphids are also seen in the bird cherry-oat aphid Rhopalosiphum padi (Nottingham et al., 1991).  Once safely air-borne, the aphids then have another set of problems to overcome.

How do they ‘decide’ when to land? How do they ‘know’ that there are host plants below them? Aphids have two main senses that help them locate their host plants, vision and smell (odour recognition) (Kring, 1972; Döring, 2014). Generally speaking, aphids respond positively to what we perceive as green or yellow light and negatively to blue and red light (Döring & Chittka, 2007) although this is not an absolute rule. Some aphids are known to preferentially choose yellowing leaves (sign of previous infestation) e.g. Black Pecan Aphid Melanocallis caryaefoliae (Cottrell et al., 2009) which indicates a pretty sophisticated host finding suite of behaviours. Aphids in flight chambers will delay landing if presented with non-host odours even in the presence of a green target (Nottingham & Hardie, 1993) and conversely can be attracted to colourless water traps that have been scented with host plant odours (Chapman et al., 1981). Aphids are thus using both visual and olfactory cues to locate their host plants and to ‘decide’ when to descend from the jet stream or boundary layer (Kring, 1972; Döring, 2014). They are not merely aerial plankton, nor are they entirely at the mercy of the winds, they do not deserve to be described as passive (Reynolds & Reynolds, 2009).

Once at ground level and on a potential host plant, aphids go through a complicated suite of behaviours to determine if the host is suitable or not; if the plant meets all the required

From air to plant – how aphids chose their host plants – after Dixon (1973).

 

criteria, then the aphid will start feeding and reproducing. It is interesting to note that although there may be a lot of aphids in the air, the number of plants on the ground that

Settled safely and producing babies 🙂

http://beyondthehumaneye.blogspot.co.uk/2012/06/aphids.html  https://simonleather.wordpress.com/wp-content/uploads/2016/04/cd0a4-aphidbirth2small.jpg

 

are infested with them is relatively low, about 10% in a diverse landscape (Staab et al., 2015), although in a crop, the level of infestation can approach 100% (e.g. Carter et al., 1980). The fact that in some cases less than 1% of those that set off will have found a host plant (Ward et al., 1998) is not a problem when you are a member of clone; as long as not all of the members of a clone gets lost the journey has been a success.

They may be small, they may be weak flyers, but enough of them find a suitable host plant to keep the clone alive and kicking; not all aphids get lost.

 

References

Carter, N., Mclean, I.F.G., Watt, A.D., & Dixon, A.F.G. (1980) Cereal aphids – a case study and review. Applied Biology, 5, 271-348.

Chapman, R.F., Bernays, E.A., & Simpson, S.J. (1981) Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. Journal of Chemical Ecology, 7, 881-888.

Cockbain, A.J. (1961) Fuel utilization and duration of tethered flight in Aphis fabae Scop. Journal of Experimental Biology, 38, 163-174.

Cottrell, T.E., Wood, B.W. & Xinzhi, N. (2009) Chlorotic feeding injury by the Black Pecan Aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environmental Entomology, 38, 411-416

David, C.T. & Hardie, J. (1988) The visual responses of free-flying summer and autumn forms of the black bean aphid, Aphis fabae, in an automated flight chamber. Physiological Entomology, 13, 277-284.

Dixon, A.F.G. (1971) Migration in aphids. Science Progress, Oxford, 59, 41-53.

Dixon, A.F.G. (1973) Biology of Aphids, Edward Arnold, London.

Döring, T.F. & Chittka, L. (2007) Visual ecology of aphids – a classcial review on the role of colours in host finding. Arthropod-Plant Interactions, 1, 3-16.

Döring, T., Hardie, J., Leather, S.R., Spaethe, J., & Chittka, L. (2008) Can aphids play football? Antenna, 32, 146-147.

Döring, T. (2014) How aphids find their host plants, how they don’t. Annals of Applied Biology, 165, 3-26.

Elton, C.S. (1925) The dispersal of insects to Spitsbergen. Transactions of the Entomological Society of London, 73, 289-299.

Gislen, T. (1948) Aerial plankton and its conditions of life. Biological Reviews, 23, 109-126.

Haine, E. (1955) Aphid take-off in controlled wind speeds. Nature, 175, 474-475

Johnson, C.G. (1951) The study of wind-borne insect populations in relation to terrestrial ecology, flight periodicity and the estimation of aerial populations. Science Progress, 39, 41-62.

Johnson, C.G. (1954) Aphid migration in relation to weather. Biological Reviews, 29, 87-118

Kennedy, J. S., Booth, C. O. & Kershaw, W. J. S. (1961). Host finding by aphids in the field III Visual attraction. Annals of Applied Biology, 49, 1-21.

Kring, J.B. (1972) Flight behavior of aphids. Annual Review of Entomology, 17, 461-492.

Lewis, T. (1964) The effects of shelter on the distribution of insect pests. Scientific Horticulture, 17, 74-84

Loxdale, H. D., Hardie, J., Halbert, S., Foottit, R., Kidd, N. A. C. &Carter, C. I. (1993).The relative importance of short-range and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society, 68, 291-312.

Nottingham, S.F., Hardie, J. & Tatchell, G.M. (1991) Flight behaviour of the bird cherry aphid, Rhopalosiphum padi. Physiological Entomology, 16, 223-229.

Reynolds, A.M. & Reynolds, D.R. (2009)  Aphid aerial desnsity profiles are consistent with turbulent advection amplifying flight behaviours: abandoning the epithet ‘passive’. Proceedings of the Royal Society B, 276, 137-143.

Staab, M., Blüthgen, N., & Klein, A.M. (2015) Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment Oikos, 124, 827-834.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

 

Post script

Political and geographic borders are not factors that deter aphid migrants, Wiktelius (1984) points out that aphids regularly make the journey across the Baltic in both directions to and from Sweden.

Wiktelius, S. (1984) Long range migration of aphids into Sweden. International Journal of Biometeorology, 28, 185-200.

 

*Elton refers to it as North-East Land

** Johnson (1951) objects to this terminology in no uncertain terms. That said, as there are records of non-winged aphids being caught by aircraft (Kring, 1972), it does suggest that there may be some accidental migration going on.

*** The UK Met Office defines the boundary layer as “that part of the atmosphere that directly feels the effect of the earth’s surface” and goes on to say that depending on local conditions it can range in depth from a few metres to several kilometres.

Ten papers that shook my world – Way & Banks (1964) – counting aphid eggs to protect crops

The previous papers in this series (Southwood, 1961; Haukioja & Niemelä 1976; Owen & Weigert, 1976), were all ones that had an influence on my post-PhD career. This one in contrast, had a direct effect on my PhD as well as on my subsequent career, and was, I guess, greatly influential in the publication of the first book to deal with the ecology of insect overwintering (Leather, Walters & Bale, 1993). In 1964 Mike Way, one of the early proponents of Integrated Pest Management (in fact considered to be the father of UK IPM), was working on control methods for the black bean aphid, Aphis fabae.

Mike had recently joined Imperial College from Rothamsted Research Station where he had been leading research on ways to reduce pesticide use by farmers and growers.   During his time at Rothamsted he had worked closely with a colleague, C.J. Banks on the black bean aphid including studies on the overwintering eggs. As they said in the introduction to their paper, published four years after their experiments; “During the British winter A. fabae survives almost exclusively in the egg stage. Egg mortality might therefore be important in affecting size of populations of this species and in predicting outbreaks”. They investigated the effects of temperature and predators on the mortality of the eggs on the primary host, spindle, Euonymus europaeus, and concluded that the levels of mortality seen would not affect the success of the aphids the following spring. By 1968 (Way & Banks, 1968) they had followed up on the idea and began to feel confident that aphid populations on field beans could be predicted from the number of eggs on the winter host; spindle bushes. The publication of this paper stimulated the setting up of a long-term collaborative project monitoring Aphis fabae eggs on spindle bushes at over 300 locations throughout England south of the River Humber, and monitoring aphid numbers in about 100 bean fields per year.   In 1977 the results were finally published (Way et al., 1977) and the highly successful black bean aphid forecasting system was born. This was further refined by using the Rothamsted aphid suction trap data (Way et al., 1981).

This was also the year that I began my PhD at the University of East Anglia, working on the bird cherry-oat aphid, Rhopalosiphum padi. In the course of my preparatory reading I came across Way & Banks (1964) just in time to set up a plot of bird cherry saplings which I monitored for the next three winters, the first winter’s work resulting in my first publication (Leather, 1980). I subsequently went on to develop the bird cherry aphid forecasting system still used in Finland today (Leather & Lehti, 1981; Leather, 1983; Kurppa, 1989).

Sadly, despite the great success of these two systems there has not been a huge take-up of the idea, although the concept has been looked at for predicting pea aphid numbers in Sweden (Bommarco & Ekbom, 1995) and rosy apple aphids in Switzerland (Graf et al., 2006). Nevertheless, for me this paper was hugely influential and resulted in me counting aphid eggs for over 30 years!

References

Bommarco, R. & Ekbom, B. (1995) Phenology and prediction of pea aphid infestations on pas. International Journal of Pest Management, 41, 101-113

Graf, B., Höpli, H.U., Höhn, H. and Samietz, J. (2006) Temperature effects on egg development of the rosy apple aphid and forecasting of egg hatch. Entomologia Experimentalis et applicata, 119, 207-211

Haukioja, E. & Niemela, P. (1976) Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station, 13, 44-47.

Kurppa, S. (1989) Predicting outbreaks of Rhopalosiphum padi in Finland. Annales Agriculturae Fenniae 28: 333-348.

Leather, S. R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur Angewandte Entomolgie 96: 282-287.

Leather, S. R. & Lehti, J. P. (1981) Abundance and survival of eggs of the bird cherry-oat aphid, Rhopalosiphum padi in southern Finland. Annales entomologici Fennici 47;: 125-130.

Leather, S.R., Bale, J.S., & Walters, K.F.A. (1993) The Ecology of Insect Overwintering, First edn. Cambridge University Press, Cambridge.

Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492.

Southwood, T.R.E. (1961) The number of species of insect associated with various trees. Journal of Animal Ecology, 30, 1-8.

Way, M.J. & Banks, C.J. (1964) Natural mortality of eggs of the black bean aphid Aphis fabae on the spindle tree, Euonymus europaeus L. Annals of Applied Biology, 54, 255-267.

Way, M. J. & Banks, C. J. (1968). Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter Euonymus europaeus L. Annals of Applied Biology 62, 177-197.

Way, M. J., Cammel, M. E., Taylor, L. R. &Woiwod, I., P. (1981). The use of egg counts and suction trap samples to forecast the infestation of spring sown field beansVicia faba by the black bean aphid, Aphis fabae. Annals of Applied Biology 98: 21-34.

Way, M.J., Cammell, M.E., Alford, D.V., Gould, H.J., Graham, C.W., & Lane, A. (1977) Use of forecasting in chemical control of black bean aphid, Aphis fabae Scop., on spring-sown field beans, Vicia faba L. Plant Pathology, 26, 1-7.

 

Post script

Michael Way died in 2011 and is greatly missed by all those who knew him well. He examined my PhD thesis, and to my delight and relief, was very complimentary about it and passed it without the need for corrections. I was greatly honoured that a decade or so later I became one of his colleagues and worked alongside him at Silwood Park. He was a very modest and self-deprecating man and never had a bad word to say about anyone. He had a remarkable career, his first paper published in 1948 dealing the effect of DDT on bees (Way & Synge, 1948) and his last paper published in 2011 dealing with ants and biological control (Seguni et al., 2011), a remarkable 63 year span. His obituary can be found here http://www.telegraph.co.uk/news/obituaries/science-obituaries/8427667/Michael-Way.html

Not all aphids take the same risks

In 1970 an entomologist working on the black bean aphid, Aphis fabae, at Rothamsted Experimental Station (as it then was),  noted that he could categorise the winged individuals as either migrants, flyers or non-flyers; the former flying before they reproduced, the second flying after they reproduced and the final category, never flying (Shaw, 1970).  To describe this phenomenon he used the phrase “migratory urge” a term previously only used in the ornithological literature.

A few years later a group of PhD students in Tony Dixon’s lab at the University of East Anglia started dissecting aphids and counting their ovarioles, finding that unlike most other insects, ovariole number was variable within a species and not related to adult weight (Dixon & Dharma, 1980; Wellings et al., 1980; Leather, 1983).  Generally speaking, in insects, including aphids, the heavier they are, the more fecund they are, although in some instances this is not always true (Leather, 1988).

Figure 1 taken from http://www.aphidsonworldsplants.info/Cloning_Experts_3.htm

Figure 2 What aphid ovarioles really look like Dombrovsky  et al. BMC Research Notes 2009 2:185   doi:10.1186/1756-0500-2-185

What we found then (Wellings et al., 1980), and later (Leather et al., 1988), was that aphids with wings (alatae) even those from the same clone, had much more variability in the number of ovarioles contained within them than those without wings (apterae) (Leather et al., 1988), and that the more ovarioles an aphid contained the more fecund it was, although as mentioned earlier the number of ovarioles appeared to be independent of weight (Leather & Wellings, 1981).

So what does this have to do with migratory urge in Aphis fabae? In the early 1980s Keith Walters was working on migration in cereal aphids (Sitobion avenae and Rhopalosiphum padi) and discovered, that as with Aphis fabae these two species also produced alatae with different flight attributes (Walters & Dixon, 1983).  Building on what we in our group had discovered about ovarioles, Keith was able to show that the degree of migratory urge in aphids was determined by the number of ovarioles they contained. The greater the number of ovarioles the more reluctant they were to take flight (Figure 3ab).

Figure 3a Relationship between number of ovarioles and time to take-off (minutes) in Sitobion avenae  (Drawn from data in Walters & Dixon, 1983).

Figure 3b Relationship between number of ovarioles and time to take-off (minutes) in Rhopaloisphum padi  (Drawn from data in Walters & Dixon, 1983).

 He also found that the fewer the number of ovarioles, the steeper the angle of take-off was (Figure 4) i.e. aphids with few ovarioles climbed faster and more steeply and were thus more likely to end  up higher in the air, and thus more likely to travel further than those

Figure 4 Relationship between number of ovarioles and angle of take-off (degrees) in Rhopalosiphum padi (drawn from data in Walters & Dixon, 1983).

taking off at a shallower angle.  He also showed that resistance to starvation was greater in those aphids with fewer ovarioles and that they could also fly for longer periods of time.  Given that alatae of Aphis fabae also have a variable number of ovarioles, 6-12 (Leather et al., 1988), we can see that this fits in very well with Shaw’s classification of migrants, flyers and non-flyers.

This is yet another great example of the flexibility (plasticity) of the aphid clone.  By producing offspring that have different flight capabilities and propensities, the clone is able to hedge its bets in times of adversity; alate aphids in many aphid species are produced in response to crowding and/or poor nutritional quality (Dixon, 1973).  This deterioration in living conditions could be very local i.e. restricted to the plant on which the aphid is feeding or its immediate neighbours, slightly more widespread, i.e. at a field scale or at a much more widespread landscape scale.  Given that long distance aphid migration is very costly (only a tiny proportion survive, Ward et al, 1998) the best option is to spread the risk between the members of your clone.  Those individuals with more ovarioles and greater potential fecundity make the low risk short-distance hops (trivial flights), but take the chance that the next door plant might be just as bad as the one left behind and also within easy reach of natural enemies, but with a higher chance of arriving and reproducing.

A risk taking aphid!

 

At the other end of the scale, those clone members with fewer ovarioles and reduced potential fecundity make the long distance migratory flights, with the risk of not finding a suitable host plant in time, but with the chance that if they do, it will be highly nutritious and natural enemy-free.  A really good example of not putting all your eggs in one basket and yet again a demonstration of what fantastic insects aphids are 😉

 

References

Dixon, A.F.G. (1973) Biology of Aphids Edward Arnold, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14.

Leather, S.R. (1983) Evidence of ovulation after adult moult in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 33, 348-349.

Leather, S. R. (1988). Size, reproductive potential and fecundity in insects: Things aren’t as simple as they seem. Oikos 51: 386-389.

Leather, S.R. & Welllings, P.W. (1981) Ovariole number and fecundity in aphids. Entomologia experimentalis et applicata, 30, 128-133.

Leather, S.R., Wellings, P.W., & Walters, K.F.A. (1988) Variation in ovariole number within the Aphidoidea. Journal of Natural History, 22, 381-393.

Shaw, M.J.P. (1970) Effects of population density on the alienicolae of Aphis fabae Scop.II The effects of crowding on the expression of migratory urge among alatae in the laboratory. Annals of Applied Biology, 65, 197-203.

Walters, K.F.A. & Dixon, A.F.G. (1983) Migratory urge and reproductive investment in aphids: variation within clones. Oecologia, 58, 70-75.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

 

Not all aphids aggregate in clumps

There is a tendency for people when they do think of aphids, to see them as existing in large unsightly aggregations, oozing sticky honeydew, surrounded by their shed skins and living in positively slum-like conditions. The bird cherry-oat aphid, Rhopalosiphum padi, the black bean aphid, Aphis fabae, the Poa-feeding aphid, Utamphorophora humboldti and the beech wooly aphid, Phyllaphis fagi, being notable examples.

                                         

Whilst this may be true for many pest aphid species, it is far from true for the group as a whole. Yes they may occur in aggregations, but quite often, they look very neat and tidy and well-behaved.

    

Some aphid species lead quite solitary lives and you often only find them in ones and twos, if at all, e.g. Monaphis antennata.  There is one aphid species, however, that manages to have it both ways, living surrounded by its friends and relatives but managing to exist in splendid isolation at the same time. The exemplar of this phenomenon is the sycamore aphid, Drepanosiphum platanoidis, which exhibits a behaviour termed ‘spaced-out gregariousness’, a term coined by John Kennedy and colleagues in 1967, although the phenomenon was

described and measured by Tony Dixon a few years earlier. Effectively, the aphids like to be in a crowd but to have their own personal space. As proof of this, when the numbers of aphids on a leaf are low, say two to three, they will, instead of spreading out across the leaf, still show the same behaviour, i.e. get to within 2-3 millimetres distance of each other.

Even more extraordinary is when a predator such as a ladybird or lacewing larvae finds its way on to a crowded leaf; the sycamore aphids do a great imitation of the parting of the Red Sea, but still without touching each other and keeping their regulation distance apart. Those finding themselves at the edge, either take wing or move to the upper surface of the leaf. Although a video of this exists somewhere I have been unable to find it so you will have to take my word for it. If anyone does come across the footage please let me know.

Yet another reason to love aphids.

 

References

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Kennedy, J.S., Crawley, L., & McLaren, A.D. (1967) Spaced-out gregariousness in sycamore aphids Drepanosiphum platanoides (Schrank) (Hemiptera, Callaphididae). Journal of Animal Ecology, 36, 147-170.

Post script 

You may have noticed that the two references cited spell the species name of the sycamore aphid as platanoides,  It is in fact correctly spelt platanoidis.  To their embarrassment both John Kennedy and Tony Dixon got it wrong.  It wasn’t until 1978, when a very brave (possibly helped by conference alcohol consumption) PhD student (David Mercer) of Tony Dixon’s pointed this out, that the error was noticed and corrected 😉

Reference

Mercer, D.R. (1979) Flight Behaviour of the Sycamore Aphid, Drepanosiphum platanoidis Schr.   Ph.D Thesis, University of East Anglia, Norwich, UK.

 

Entomological classics – The clip cage

Mention clip cage to an aphidologist and the chances are that they will smile and begin reminiscing about the days when they had to sit down and spend hours refurbishing and making new ones; if they were lucky enough to be in a big research group as I was, they will have had the fun of the communal clip cage renovation day, otherwise they will have laboured doggedly away on their own.  Mention clip cage to an entomologist and they may have heard of them, but probably not used them; to a non-entomologist you will be talking gibberish.  In fact, this week at the beginning of a lecture to the MSc Entomology course here at Harper Adams, I held a clip cage in the air and asked those who knew what it was to put their hands in the air, less than a third were willing to hazard a guess.  For those of you who don’t know the answer, clip cages were invented, or at least revealed in the scientific literature by two Canadian entomologists MacGillivray & Anderson in 1957.  Their purpose, to keep aphids confined individually to leaves of a plant in a simple and effective way.

Before this aphidologists generally used to confine them in large cages covering whole plants, (Davidson, 1925; Kennedy & Booth, 1950).  This allowed the aphids to select their own feeding sites but which of course made knowing what an individual aphid was doing in terms of longevity and fecundity quite difficult.  Kennedy & Booth (1950) were very much aware of this and attempted to solve the problem by using this using this rather over-engineered reproduction cage

This cage, although doing the job was difficult to make and also required a somewhat complicated method of attachment to the plant so as not to pull the leaves off, hence the birth of the

MacGillivray  and Anderson clip cage.  In 1958 another Canadian entomologist Noble described a variant on the MacGillivray & Anderson version where instead of a muslin lid, a cork was used , the theory being that you didn’t need to open the clip to check what the aphid was doing and risk it falling off the leaf, something aphids seem to delight in doing , especially when you are six

 

 days into obtaining seven-day fecundity readings!  Incidentally, this version of the clip cage has resulted in one of my favourite bug-bears, as many people tend to cite Noble (1958) when referring to clip cages, that is if they actually remember to cite anyone at all, and of course they are using the MacGillivray & Anderson version.

Since then the humble clip cage has become the standard way for aphidologists to keep aphids on single leaves of their hosts plants.  They have also been used to confine young Lepidopteran larvae to leaves (Moore et al, 2003) but due to the frass production of lepidopteran larvae are better suited to aphids whose honeydew causes less of a problem for cage cleanliness.  They are very versatile and can be made in different sizes to suit the host plant.   All you need are hair clips,  Perspex tubing and the wherewithal to cut it to the right size, some foam or sponge, fine muslin or  similar textile and a waterproof adhesive.

     

Clip cages are not perfect. There are some drawbacks;  for example, if you don’t move them slightly every day the leaves can develop chlorosis which of course will change the performance of the  aphids  and there is some evidence that the leaf can suffer some physical damage (Moore et al,  2003) and that even if you do move the cages the aphids can behave slightly differently than those in  whole plant cages (Awmack & Leather (2007), but as long you are aware of the possible drawbacks  clip cages remain an indispensable tool for those wishing to study single aphids on whole plants.

And of course, there is the immense satisfaction and sense of achievement of being able to make your own equipment relatively simply and inexpensively.  That said, I certainly received some strange looks when I was working in  Finland and found that there were no clip cages in the lab and had to attempt to buy hair clips in  down-town Helsinki.

Awmack, C. S. & Leather, S. R. (2007).Growth and development. In Aphids as Crop Pests, 135-151 (Eds H. F. Van Emden and R. Harrington). Wallingford: CABI.

Davidson, J. (1925) Biological studies of Aphis ruimicis Linn. factors affecting the infestation of Vicia faba with Aphis rumicis.  Annals of Applied Biology, 12, 472-507

Evans, A.C. (1938) Physiological relationships between insects and their host plants I. The effect of the chemical composition of the plant on reproduction and production of winged forms in Brevicoryne brassicae L. (Aphididae).  Annals of Applied Biology, 25, 558-572

Kennedy, J.S. & Booth, C.O. (1950) Methods for mass rearing and investigating the host relations of Aphis fabae Scop.  Annals of Applied Biology, 37, 451-470

MacGillivray, M. E. &Anderson, G. B. (1957). Three useful insect cages. Canadian Entomologist 89: 43-46.

Noble, M. D. (1958). A simplified clip cage for aphid investigations. Canadian Entomologist 90, 60.

Moore, J.P., a, J.E., Paul, N.D. & Whittaker, J.B. ( 2003)  The use of clip cages to restrain insects    reduces leaf expansion systemically in Rumex obtusifolius Ecological Entomology, 28, 239-242

Aphid life cycles – bizaare, complex or what?

In a very early post I mentioned that one of the reasons that I love aphids so much is their life-cycles https://simonleather.wordpress.com/aphidology/  and the fantastic jargon that is used to describe them.  Many undergraduates find the jargon off-putting but it was this complexity that really grabbed my imagination.

Insects are probably the most diverse group of organisms on Earth (Grimaldi & Engel, 2005) and their life cycles range from simple sexual and asexual styles to complex life cycles encompassing obligate and facultative alternation of sexual and asexual components.  Nancy Moran (1992) suggests that in the insect world probably the most intricate and varied life cycles are found in aphids and I certainly wouldn’t disagree.

There are basically two types of aphid life-cycles, non-host alternating (autoecious, monoecious) and host alternating (heteroecious).   Autoecious aphids spend their entire life cycle in association with one plant species as shown below (Dixon, 1985).

(or group of related plant species), whereas heteroecious aphids divide their time between two very different species of host plant, usually a tree species (the primary host) on which they overwinter, and an herbaceous plant species (the secondary host) on which they spend their summer.

Approximately 10% of aphid species are heteroecious.  The ancestral aphid life cycle is thought to have been winged, egg laying and autoecious on a woody host plant almost certainly conifers and the oldest families of woody angiosperms e.g. Salicaceae (Mordwilko, 1928; Moran, 1992).

Aphid life cycles can also be described as holocyclic, in which cyclical parthenogenesis occurs, with aphids reproducing sexually in the autumn to produce an overwintering egg, in temperate regions and parthenogenetically during spring and summer as shown below for the sycamore aphid (Dixon, 1985).

Some aphids are anholocyclic where the clone is entirely asexual reproducing by parthenogenesis throughout the year. This is often seen in locations where winter conditions are mild, in the tropics for example or as a bit of an oddity around hot-springs in Iceland.

Parthenogenesis in aphids is coupled with live births and reduced generation times through the phenomenon of telescoping generations.  Parthenogenesis in aphids developed early on but whether the oldest aphids (200 mya) were parthenogenetic is not known.

Host alternation appears to have arisen more than once (Moran, 1988), and occurs in four slightly different forms depending on the taxon in which it occurs.  The main differences being in whether the sexual forms are produced on the primary (winter) host (the host on which the eggs are laid), or as in the case of the Aphidini, the males being produced on the secondary (summer) host and the sexual females produced on the primary host.   The majority of aphids host alternate between unrelated woody and perennial hosts, but some species host alternate between herbaceous plants e.g. pea aphid Acyrthosiphon pisum alternates between the perennial vetches and the annual peas Pisum sativum (Muller & Steiner, 1985) and Urleucon gravicorne alternates between the perennial Solidago and the annual Erigeron (Moran 1983).  Some aphid species such as Rhopalosipum padi, have clones that are holocyclic and some that are anholocyclic, so hedge their bets and also gives me the opportunity to slip in a great slide kindly lent to me by my friend Richard Harrington at Rothamsted Research.

One of the things that is rather puzzling is why some aphid species should have adopted a host alternating life cycle which on the face of it, seems to be rather a risky strategy.  You could liken it to looking for a needle in a hay-stack; only about 1 in 300 aphids that leave the secondary host at the end of summer are likely to find their primary host (Ward et al, 1998).  There are a number of theories as to why it has evolved.

1. The nutritional optimization through complementary host growth hypothesis states that heteroecy has been favoured by natural selection because it enables a high rate of nutrient intake throughout the season (Davidson, 1927; Dixon, 1971).  In essence, the clone moves from a host plant where food quality is low and moves onto a herbaceous host that is growing rapidly and thus provides a good source of nutrition.  In autumn, the clone moves back to its primary woody host where leaves are beginning to senesce and provide a better source of nutrition as seen below (Dixon, 1985).

On the other hand, non-host alternating aphids such as the sycamore aphid, Drepanosiphum platanoidis, or the maple aphid, Periphyllus testudinaceus, reduce their metabolism and tough it out over the summer months when the leaves of their tree hosts are nutritionally poor, the former as adults, the latter as nymphs (aphid immature forms) known as dimorphs. Mortality over the summer in these species is, however, very high.  In some years I have recorded almost 100% mortality on some of my study trees, so very similar to the 99.4% mortality seen in the autumn migrants (gynoparae) of the bird cherry-oat aphid, Rhoaplosiphum padi.  Other autoecious aphids are able to track resources if they live on host plants that continue to develop growing points throughout the summer.

 

Verdict:  No apparent advantage gained

2. The oviposition site advantage hypothesis states that primary woody hosts provide better egg laying sites and provide emerging spring aphids with guaranteed food source (Moran, 1983).  There is however, no evidence that eggs laid on woody hosts survive the winter better than those laid in the herbaceous layer.  Egg mortality in both situations ranges from 70-90% (Leather, 1983, 1992, 1993).

Verdict:  No apparent advantage gained

3.  The enemy escape hypothesis states that by leaving the primary host as natural enemy populations begin to build up and moving to a secondary host largely devoid of enemies confers an advantage on those species that exhibit this trait (Way & Banks, 1968).  At the end of summer, when the natural enemies have ‘found’ the clone again, the clone then migrates back to its primary host, which theoretically is now free of natural enemies.  This is an attractive idea as it is well known that natural enemies tend to lag behind the populations of their prey.

Verdict: Possible advantage gained

4. The Rendez-vous hosts hypothesis suggests that host alternation assists mate location and enables wider mixing of genes than autoecy (Ward, 1991; Ward et al. 1998).  This seems reasonable, but as far as I know, no-one has as yet demonstrated that host-alternating aphid species have a more diverse set of genotypes than non-host alternating aphids.

Verdict:  Not proven

5.  The temperature tolerance constraints hypothesis which postulates that seasonal morphs are adapted to lower or higher temperatures and that they are unable to exist on the respective host plants at the ‘wrong time of year’ (Dixon, 1985).  I don’t actually buy this one at all, as I have reared spring and autumn morphs at atypical temperatures and they have done perfectly well (Leather & Dixon, 1981), the constraint being the phenological stage of their host plant rather than the temperature.  In addition, there are some host alternating aphid species in which the fundatrix can exist on both the secondary and primary hosts (if the eggs are placed on the secondary host).  This has been experimentally demonstrated in the following species:

Aphis fabae                                 Spindle & bean                                        Dixon & Dharma (1980)

Cavariella aegopdii

Cavariella pastinacea              Willows and Umbelliferae                     Kundu & Dixon (1995)

Cavariella theobaldi

Metopolophium dirhodum       Rose and grasses                                    Thornback (1993)

Myzus persicae                           Prunus spp &  40 different plants       Blackman & Devonshire (1978)

Verdict: Unlikely

6.  The escape from induced host-plant defences hypothesis (Williams & Whitham, 1986), which states that by leaving the primary host as summer approaches, the aphids escape the plant defences being mustered against them.  This is only really applicable to those gall aphids where galled leaves are dropped prematurely by the host plant.

Verdict: Special case pleading?

7.  The constraint of fundatrix specialisation hypothesis is that of Moran (1988), who argues that heteroecy is not an optimal life cycle but that it exists because the fundatrix generation (the first generation that hatches from the egg in spring) on the ancestral winter host, are constrained by their host affinities and are unable to shift to newly available nutritionally superior hosts.  Whilst it is true that some host alternating aphids are however, very host specific as fundatrcies, some aphids are equally host-specific as oviparae at the end of the year the constraints of ovipara specialisation

For example, in the bird cherry-oat aphid Rhopalosiophum padi, the fundatrices are unable to feed on senescent leaf tissue of the primary host, their offspring can only develop very slowly on ungalled tissue and all their offspring are winged emigrants (the alate morph that flies from the primary host to the secondary host) (Leather & Dixon, 1981).  The emigrants are able to feed as nymphs on the primary host on which they develop and as adults on their secondary host, but not vice versa (Leather et al., 1983).  The autumn remigrants (gynoparae, the winged parthenogenetic females that fly from the secondary hosts to the primary hosts on the other hand, feed on the secondary host as nymphs but are unable to feed on the primary host as adults (Leather, 1982; Walters et al., 1984).  The black bean aphid shows similar, but less rigid host specificity and whilst there is a distinct preference for the relevant host plant (Hardie et al., 1989), parthenogenetic forms can occur throughout the summer on the primary host (Way & Banks, 1968), particularly if new growth is stimulated by pruning (Dixon & Dharma, 1980). There are also at least two examples of where both the primary and secondary host are herbaceous (see earlier).  In both these cases the fundatrices could exist on both the primary and secondary host plants

Verdict:  Not proven

So what do I think?  For years I was very firmly convinced that the nutritional optimization hypothesis was the obvious answer; after all Tony Dixon was my PhD supervisor 😉  Now, however, having lectured on the subject to several cohorts of students, if I was forced to pick a favourite from the list above, I would do a bit of fence-sitting and suggest a combination of the nutritional optimization and enemy escape hypotheses. What do you think? There are cetainly a number of possible research projects that would be interesting to follow up, the problem is finding the funding 😦

Sources

Blackman, R.L. & Devonshire, A.L. (1978)  Further studies on the genetics of the carboxylase-esterase regulatory system involved in resistance to orgaophosphorous insecticides in Myzus persicae (Sulzer).  Pesticide Science 9, 517-521

Davidson, J. (1927) The biological and ecological aspects of migration in aphids.  Scientific Progress, 21, 641-658

Dixon, A.F.G. (1971) The life cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi (L) and its bearing on the theory of host alternation in aphids. Annals of  Applied Biology, 68, 135-147.  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1971.tb06450.x/abstract

Dixon, A.F.G. (1985) Aphid Ecology Blackie, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1980.tb02981.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Grimaldi. D. & Engel, M.S. (2005)  Evolution of the Insects, Cambridge University Press, New York

Hardie, J. (1981) Juvenile hormone and photoperiodically controlled polymorphism in Aphis fabae: postnatal effects on presumptive gynoparae. Journal of Insect Physiology, 27, 347-352.

Hardie, J. Poppy, G.M. & David, C.T. (1989) Visual responses of flying aphids and their chemical modification. Physiological Entomology, 14, 41-51.  http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3032.1989.tb00935.x/abstract

Kundu, R. & Dixon, A.F.G. (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology, 64, 245-255.  http://www.jstor.org/discover/10.2307/5759?uid=3738032&uid=2&uid=4&sid=21102533364873

Leather, S.R. (1982) Do gynoparae and males need to feed ? An attempt to allocate resources in the bird cherry-oat oat aphid Rhopalosiphum padi. Entomologia experimentalis et applicata, 31, 386-390.  http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1982.tb03165.x/abstract

Leather, S.R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur  Angewandte  Entomolgie, 96, 282-287. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1983.tb03670.x/abstract

Leather, S.R. (1992) Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis, 17, 101-113.  http://www.cabdirect.org/abstracts/19941101996.html;jsessionid=60EA025C7230C413B6094BCC4966EC06

Leather, S.R. (1993) Overwintering in six arable aphid pests: a review with particular relevance to pest management. Journal of Applied Entomology, 116, 217-233. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1993.tb01192.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on it’s primary host. Annals of applied Biology, 99, 115-118. http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1981.tb05136.x/abstract

Moran, N.A. (1983) Seasonal shifts in host usage in Uroleucon gravicorne (Homoptera:Aphididae) and implications for the evolution of host alternation in aphids. Ecological Entomology, 8, 371-382. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2311.1983.tb00517.x/full

Moran, N.A. (1988) The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. American Naturalist, 132, 681-706. http://www.jstor.org/discover/10.2307/2461929?uid=3738032&uid=2&uid=4&sid=21102533364873

Moran, N.A. (1992) The evolution of aphid life cycles. Annual Review of Entomology, 37, 321-348. http://www.annualreviews.org/doi/abs/10.1146/annurev.en.37.010192.001541

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