Tag Archives: host plant quality

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 2nd, 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 🙂



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 persicaeEntomologia 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




Filed under Aphidology, Aphids

The bane of PhD students– the General Discussion

This year has been a bit of a bumper PhD submission year for me, five of my PhD students have come to the end of their time, and have submitted, or will soon be submitting their theses.  In my experience, 48 successful students and counting, it is relatively easy to reassure PhD students that their worries about the structure of their thesis, the appropriateness of their analysis and how many tables and figures they should have, are not justified. Many of them already have papers in print or in press by the writing-up stage so they only need a little bit of reassurance about the quality of their work.  The bit that seems to worry them most is the General Discussion.  My advice to them was, and is, the same as that given to me by my supervisor 37 years ago, “spread your wings, sell your work, don’t be afraid to speculate a little, enjoy yourself and make sure you don’t just summarise your thesis”. 

This uncertainty about how to handle the General Discussion is not just a foible of my students.  My impression over the last few years, borne out by the increasing frequency on which I comment on the shortcomings of the General Discussion of the PhD theses that I examine (now more than sixty) is that General Discussions are not what they used to be.  I too often find myself reading a series of lightly edited chapter abstracts, which in my opinion is not a General Discussion. Am I, however, suffering from grumpy old git syndrome or were General Discussions more general in the days of my youth?  How for example, does my General Discussion stack up compared with that of the modern-day PhD student? Did I practice what I now preach?

I do of course still have a copy of my thesis (Leather, 1980), two to be precise. Both my parents were biologists, albeit botanists, so I felt obliged to give them a copy, which I retrieved when clearing my Mother’s house after her death.  The upshot being that I have no excuse for not being able to find a copy from which to do a critical appraisal of my General Discussion. My thesis was written before Word Processors existed, and when computers occupied their own buildings. It was typewritten (by me using a Silver Reed A3 typewriter) and so no electronic copies are available.  As a consequence, I have had to scan the parts relevant to my story; hence the poor quality of the illustrations 🙂

At this point, I should point out that although I was trained as an agricultural entomologist and my PhD was about an agricultural pest, the bird cherry-oat aphid, my supervisor, Tony Dixon, was and still is, an ecologist.  Our lab was thus a mixture of pure and applied ecologists, some of whom weren’t even entomologists 🙂 This meant that I was exposed to a wider range of ideas than if I had just been in a lab of only applied entomologists.  Despite not being overly mathematical or theoretically inclined, I’m pretty much an empirical ecologist (field and lab), I was very impressed by the late, great E.C. Pielou, to the extent that I bought her book Ecological Diversity and read it cover to cover*.  Working with a host alternating aphid, I immediately latched on to her definition of seasonality as being synonymous with environmental variability (Pielou, 1975) and decided to coin a new term, seasonability** .

An excellent start, the title page doesn’t even mention the words General Discussion 🙂


I defined seasonability as being “the pre-programmed response to predictable environmental change” in  my terms this meant that the organism, in this case my aphid, anticipates the trend in conditions, something I, and a more mathematically inclined colleague did actually show a couple of years later (Ward et al., 1984).  I then drew the analogy that an aphid clone could be equated with Harper’s visualisation of a plant being constructed of a series of genetically identical modular units (Harper, 1977), i.e. each individual within the clone, although being genetically identical has a specific (and seasonal) function I also managed to slip in a reference to my other ecological hero, Dan Janzen at this point (Janzen, 1977) 🙂

I see that I was keen to introduce new terms, as my second figure shows.  I was amused to see in figure legend that I describe the x-axis as food quality but label it as host quality in the

A pretty lousy figure, but remember we had to draw our figures by hand in those days. Here I attempt to coin another new usage, this time refluence, to indicate the flowing back of the clone to the primary host.

figure, doing something that in later years I have waxed wrathfully against (Leather & Awmack, 1998; Awmack & Leather, 2002).  In this case, food (nutritional) quality is the term I should have used although I could argue that the build-up of natural enemies on the secondary grassy hosts and the predictable absence of natural enemies on the primary host, could justify the use of the term host quality, but that would be post hoc sophistry and best avoided 🙂

I was obviously also very keen to introduce new meanings to words as my third figure shows.

Yet another attempt to coin a new meaning for an existing word


At no point however, did I summarise what was in each chapter.  I referred in passing to one…”It is now fairly certain from the evidence presented on the effects of growth stage (Chapter 4) that..” and the four figures are unique to my General Discussion, even the two that contained data points, so I can pat myself on the back in that respect.  Although I did not extend my discussion to other taxa, I did range far and wide across the aphid world so I think that fulfilled the brief of spreading my wings, and boy did I try and sell my work.

I also notice that the 25-year-old me tried very hard to use a different sort of language in his General Discussion such as, “lends further credence to the concept of seasonability” which is followed in the next sentence by “..when the bursting of the buds of the tree host or resurgence of sap in the perennial herbaceous host, herald the start of egg hatch”. Yes, I actually used the word herald, but then, this is the guy who prefaced his thesis with these two quotes.

The Steinbeck quote (Doc from Sweet Thursday, does still sums up pretty much what I want to do with my life.


So what does the 62-year-old Professor of Entomology think about the efforts of his younger self?  I may be slightly biased, but I think it is a reasonable effort and as an examiner I wouldn’t have any major problems with it although I suspect that I would be tempted to have a gentle dig at the attempts to coin new terms. Overall I would rate it as B+.

In case you wondered , although I never published, or even tried to publish my General Discussion, all the ideas, except for the terms which were petty awful, (or naff as we would say in the UK), have made it into print at some time.

To reiterate, my advice to PhD students struggling with your General Discussion is “spread your wings, be bold, sell your work, don’t be afraid to speculate a little, enjoy yourself and most importantly,  definitely make sure you don’t just summarise your thesis”


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

Leather, S.R. (1980)  Aspects of the Ecology of the Ecology of the Bird Cherry-Oat Aphid, Rhopalosiphum padi (L.).  Unpublished PhD Thesis, University of East Anglia, Norwich.

Leather, S.R. & Awmack, C.S. (1998). The effects of qualitative changes of individuals in the population dynamics of insects. In Insect Populations In Theory and in Practice (ed. by J.P. Dempster & I.F.G. McLean), pp. 187-206. Kluwer, Dordrecht.

Harper, J.L. (1977) Plant Population Biology, Academic Press, London.

Janzen, D. H. (1977) What are dandelions and aphids? American Naturalist, 111, 586-589.

Pielou, E.C. (1975) Ecological Diversity, John Wiley & Sons Inc., New York.

Ward, S.A., Leather, S.R., & Dixon, A.F.G. (1984) Temperature prediction and the timing of sex in aphids. Oecologia, 62, 230-233.


*I also bought her book Mathematical Ecology but didn’t manage to read it cover to cover 🙂

**I had great hopes of getting my General Discussion published and my new term being adopted by ecologists around the world 🙂


Filed under Science writing, Teaching matters