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

 

Ten papers that shook my world – Lewis (1969) – the importance of (h)edges for natural biological control

In 1969, Trevor Lewis, of what was then the Rothamsted Research Station (now Rothamsted Research), published two landmark papers (Lewis 1969ab). These papers, in which he described the importance of hedges as habitats for insects (Lewis, 1969a) and in acting as possible sources of natural enemies able to colonise nearby fields (Lewis, 1969b) were to have a profound effect on me and generations of applied entomologists and pest mangers to the present day.

In 1976 the UK experienced what is now recognised as the warmest year of the 20^th Century.  It was also the year that I started my final year as an undergraduate.  Before entering our final year we had to do a research placement or project.   I opted to do my project at home, I was making very good money as a temporary postman and as I usually finished my round by 10 am, I had plenty of time during the rest of the day to get to grips with my project.  I had come across the Lewis papers in lectures and thought that it would be interesting to do a similar study; given the weather I was also keen to spend as much time outside as possible 🙂 My Uncle James owned a local farm and was happy for me to sample some of his hawthorn hedges, so sampling hawthorn hedges was what I did during July and August of the glorious summer.

The intrepid student entomologist; trusty bike, clipboard and a copy of Chinery*. Note the wellington boots despite the heat 🙂

The hedges in question – three types of management

As I mentioned earlier, 1976 was the warmest year on record at the time, and I see from my report that during August I was recording temperatures in excess of 25^oC, even in the hedge bottoms.

The report

What is interesting is that although 1976 was one of the famous ladybird outbreak years (in fact last week I was interviewed by the BBC about my memories of that very same event) I didn’t record more than a handful of ladybirds in my surveys.  Perhaps inland Yorkshire just wasn’t attractive enough 🙂

Overall my results showed that over-clipping resulted in more crop pests being present and that hedges with less clipping supported a greater diversity of insect life than the more managed ones, very similar to results being reported today (e.g Amy et al., 2015).

Sadly, although Lewis’s two 1969 papers and to a certain extent his earlier paper in a much harder to access source (Lewis, 1964), led on to the concept of conservation headlands (Sotherton et al., 1989) and ‘crop islands’ (Thomas et al., 1991), which are an integral part of European Union subsidised farm payments, it was included in an influential review article (van Emden & Williams, 1974).  As pointed out recently by Terry McGlynn over at Small Pond Science, this often rings the death knell for a paper’s citation score.  As a result,  Lewis (1969b) has only been cited 91 times since 1969 and is barely remembered at all.   I remember being invited to be a facilitator at a Populations Under Pressure conference workshop on this very subject at the NERC Centre for Population Biology at Silwood Park about fifteen years ago and being surprised that none of the participants had even heard of Trevor Lewis let alone read his papers.

At the Populations Under Pressure conference brandishing my undergraduate hedgerow report!

The subject of hedgerow and crop edge management is still a highly important research area today, and you will be pleased to know that in the latest paper just submitted from my research group, we cite both of Trevor’s 1969 papers. Hopefully this will do something to redress the balance and bring Trevor some of the recognition that he deserves, however belated.

 

References

Amy, S.R., Heard, M.S., Hartley, S.E., George, C.T., Pywell, R.F. & Staley, J.T. (2015) Hedgerow rejuvenation management affects invertebrate communities through changes to habitat structure. Basic & Applied Ecology, 16: 443-451

Chinery, M. (1973) A Field Guide to the Insects of Britain and Northern Europe.  Collins, London

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

Lewis, T. (1969a). The distribution of flying insects near a low hedgerow. Journal of Applied Ecology 6: 443-452.

Lewis, T. (1969b). The diversity of the insect fauna in a hedgerow and neighbouring fields. Journal of Applied Ecology 6: 453-458.

Sotherton, N.W., Boatman, N.D. & Rands, M.R.W. (1989) The “Conservation Headland” experiment in cereal ecosystems. The Entomologist, 108: 135-143

Thomas, M.B., Wratten, S.D., & Sotherton, N.W. (1991) Creation of ‘island’ habitats in farmland to manipulate populations of beneficial arthropods: predator densities and emigration. Journal of Applied Ecology, 28: 906-917.

Van Emden, H.F. & Williams, G.F. (1974) Insect stability and diversity in agro-ecosystems. Annual Review of Entomology, 19: 455-475

*I still own that copy of Chinery which was a present for my 20^th birthday – take note of the date if anyone wants to send me a present or card 🙂

 

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Not all aphids taste the same

One morning sometime in the late 1970s, when I was doing my PhD at the University of East Anglia, I walked into the lab to find one of my fellow PhD students sitting in front of a row of Petri dishes filled with different species of aphids.  Curious, I asked him what he was doing.  His reply was that he was tasting the aphids to see why his ladybirds made the choices they did.  This was a guy whose hobby was collecting and identifying Chamaemymiid flies, so I was not entirely surprised, although I did point out that it was unlikely his taste receptors and those of the two-spot ladybird (Adalia bipunctata) had a lot in common.

That said, his premise that aphids don’t all taste the same was of course perfectly correct.  Aphid predators, in particular ladybirds, seem to have quite strong preferences for different aphid species and these preferences are strongly correlated with larval development and subsequent fecundity as adults (Kalushkov, 1998; Kalushkov & Hodek, 2004).  What is perhaps not as well-known is that certain aphids, like many lepidopteran larvae, are extremely good at sequestering potentially toxic chemicals from their host plants.  Over a century ago, Johnson (1907) noted that highly coloured and woolly (in this case meaning waxy) aphids were not eaten as readily as smoother, greener aphids.  Half a century later Hodek (1956, 1957), showed that larvae of the seven spot ladybird (Coccinella septempunctata) were unable to complete their development if fed a diet of the elder aphid Aphis sambuci and that young adult ladybirds died if fed on the same diet.  Note that A. sambuci although not brightly coloured has waxy plaques on its abdomen.

Aphis sambuci  http://aramel.free.fr/INSECTES10-4′.shtml

The mealy plum aphid, Hyalopterus pruni, although bright green, is also waxy, and when attacked by larvae of the ten spot ladybird, Adalia decempunctata, is released as oon as the ladybird larva comes into contact with the aphid’s haemolymph (insect blood) (Dixon, 1958).

Hyalopterus pruni, the mealy plum aphid http://influentialpoints.com/Gallery/Hyalopterus_pruni_Mealy_Plum_Aphid.htm

The vetch aphid Megoura viciae, on the other hand, is rather a handsome dark green aphid, with startlingly red eyes.  If however, a larva of the ten-spot ladybird is foolish enough to eat

Megoura viciae, the vetch aphid  http://influentialpoints.com/Gallery/Megoura_aphids.htm

one, it will, after about two minutes, be violently sick.  Those are the lucky ones; those that don’t regurgitate the aphid are very likely to die a few days later.  The two spot aphid, Adalia bipuncatata is also killed if it is unlucky enough to eat M. viciae (Blackman, 1967).  It appears that the vetch aphid is full of all sorts of interesting and potentially fatal chemicals (Dixon et al., 1965). Truly a toxic treat.  Megoura viciae is not the only toxic aphid out there.  Aphis craccivora, the cowpea aphid, is a beautiful mahogany brown aphid, but despite its attractive

Aphis craccivora, the cowpea aphid

appearance, it is extremely toxic to the eleven spot ladybird Semiadalia undecimnotata, although the seven spot ladybird finds it perfectly acceptable (Hodek, 1970).

A similar effect is seen with the cabbage aphid, Brevicoryne brassicae, which is extremely good at sequestering glucosinolates, especially sinigrin, from its Brassica host plants.  Glucosinolates are the compounds that give cabbages and related plants, such as Brussels sprouts, their distinctive flavour.  In high dosages they can cause liver damage in young mammals, one of the reasons why children are so reluctant to eat cabbage, despite their parent’s urgings.  Brevicoryne brassicae is so good at sequestering  glucosinolates that larvae of the two spot ladybird die when fed on aphids from sinigrin rich cabbages (Kazana et al., 2007). The seven spot ladybird however, although not entirely happy when fed on a diet of sinigrin- rich cabbage aphids is able to survive, develop and reproduce successfully (Pratt et al., 2008).  It obviously has a much better detoxification system than that of the two spot ladybird which for an aphidophagous predator seems singularly specialist.

Brevicoryne brassicae – the cabbage aphid; a colony being approached by a hungry seven spot ladybird (Photo Corin Pratt & Tom Pope).

Another aphid that sequesters plant derived toxins is the Stinkvine aphid, Acyrthosiphon nipponicus, which accumulates an iridoid glycoside, paederoside from it’s host plant the stinkvine Paederia foetidae (syn = scandens) (Nishida & Fukami, 1989). This brightly coloured aphid does not have to merge into the background; its chemical defence is so strong that

Acythrosiphon nipponicus – Stinkvine or Skunk-vine aphid http://homepage3.nifty.com/MICHI_A/akigase/AKIGASEKOUEN_hannsimoku2-1.htm

even that voracious predator the Harlequin ladybird, Harmonia axyridis, turns tail when dabbed with the aphid’s siphuncular fluid, or if it is unlucky enough to bite into the aphid, drops the aphid, regurgitates and rapidly leaves the leaf on which the aphid colony is feeding.

And finally, this striking, although rather noxious yellow aphid, the oleander aphid, Aphis nerii, which very honestly advertises that it is indeed a mouthful to be avoided.

Aphis neri – the oleander aphid http://www.zenthroughalens.com/2012/01/aphis-nerii-and-i.html

Aphis nerii is packed full ofcardiac glycosides which it sequesters from its host plant(Rothschild et al., 1970) and provides a powerful defence against potential predators, not just ladybirds.

So bear in mind, that although aphids may seem to be soft-bodied, small and defenceless, many of them are extremely well defended chemically as well as behaviourally.  This suite of complex defence mechanisms may go some way to  explain the ability of aphids to keep at least one step ahead of their natural enemies.

References

Blackman, R.L. (1967) The effects of different aphid foods on Adalia bipunctata L. and Coccinella septempunctata.  Annals of Applied Biology, 59: 207-219  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1967.tb04429.x/abstract

Dixon, A.F.G. (1958) The escape responses shown by certain aphid to the presence of the coccinellid Adalia decmpunctata.  Transactions of the Royal Entomological Society London, 110: 319-334  http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2311.1958.tb00786.x/abstract

Dixon, A.F.G., Martin-Smith, M. & Subramanian, G. (1965) Constituents of Megoura viciae Buckton. Journal of the Chemical Society, 296: 1562-1564.

Hodek, I. (1956) The influence of Aphis sambuci L. as prey of the ladybird beetle Coccinella septempunctata L. Acta Societatis Zoologicae Bohemoslovacae, 20: 62-74 (in Czech)

Hodek, I. (1957) The influence of Aphis sambuci L. as prey of the ladybird beetle Coccinella septempunctata L. II. Acta Societatis Entomoligicae Cechosloveniae, 54: 10-17 (in Czech)

Hodek, I. (1970)  Coccinellids and the modern pest management. BioScience, 20:543-552

Johnson, R.H. (1907) Economic notes on aphids and coccinellids.  Southwestern Entomologist: 12: 107-118

Kalushkov, P. (1998). Ten aphid species (Sternorrhyncha: Aphididae) as prey for Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology 95: 343-349. http://www.eje.cz/scripts/viewabstract.php?abstract=412

Kalushkov, P. &Hodek, I. (2004). The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. Biocontrol 49: 21-32. http://link.springer.com/article/10.1023%2FB%3ABICO.0000009385.90333.b4

Kazana, E., Pope, T.W., Tibbles, L., Bridges, M., Picket, J.A., Bones, A.M. & Rossiter, J.T. (2007) The cabbage aphid: a walking mustard oil bomb. Proceedings of the Royal Society B., 274: 2271-2277. http://rspb.royalsocietypublishing.org/content/274/1623/2271.full

Nishida, R. & Fukami, H. (1989) Host plant iridoid-based chemical defense of an aphid, Acyrthosiphon nipponicus, against ladybird beetles.  Journal of Chemical Ecology, 15: 1837-1845  http://link.springer.com/article/10.1007/BF01012270

Pratt, C., Pope, T.W., Powell, G. & Rossiter, J.T. (2008)  Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassciae as a defence against two Coccinellid species.  Journal of Chemical Ecology, 34: 323-329 http://link.springer.com/article/10.1007/s10886-007-9421-z

Rothschild, M., von Euw, J. & Reichstein, T. (1970)  Cardiac glycosides in the oleander aphid, Aphis nerii.  Journal of Insect Physiology, 16: 1141-1145

Tinker, Tailor, Soldier Aphid!

As a follow-up to my earlier article about biting aphids https://simonleather.wordpress.com/2013/01/25/not-all-aphids-are-vegans/, I thought it would be fun to draw people’s attention to a little-known aspect of aphid biology and ecology and yet another reason for why I love aphids so much.  Tree leaves are only really good food sources for aphids in spring and autumn, when the levels of soluble nitrogen are at their highest levels in the phloem sap (Dixon, 1973).

To get around this, a number of aphid species modify the leaf tissues by forming galls.  The galls, which are induced by chemicals in the saliva of the aphid, contain cells which are higher in nitrogen than the surrounding tissues and ensure that the nutritional quality of the leaves remains high throughout the year.

Those tree-feeding aphids, such as the sycamore aphid, Drepanosiphum platanoidis, which are unable to form galls, enter summer aestivation (reduce their metabolic rates) as an adaptation to the low nitrogen levels found in summer leaves.  Amongst aphids, the Pemphigine aphids are renowned for their gall forming activities, many of which are formed along the leaf petiole.  The position of the gall along the petiole is very important, the closer the gall is to the base of a leaf, the better the quality of the food that the gall inhabitants experience.  There is thus a premium to be gained by either being first to form a gall, or, if in second place, to usurp the aphid stem mother that got there first and push her further up the leaf petiole.   We thus see two strategies.  In the first strategy, newly emerged first instar nymphs, (such as Pemphigus betae) fight each other  for the best position on the petiole (Whitham, 1979). These fights are serious affairs, and incredibly, can last for up to two days.

In the second strategy, as seen in a related species, Epipemphigus niisimae, where a gall has already been formed by an earlier arrival, the first instar nymphs fight to gain possession of this premium dwelling place.  These fights are even more vicious and protracted and can actually result in the death of the loser (Aoki & Makino, 1982).

As a further development, a number of gall-forming aphids, such as Ceratoglypnia styracicola and Hamamelistes cristafolaie, have a specially adapted nymphal morph, with thicker and broader front legs, whose function is to defend gall usurpation by other aphid stem mothers, so-called soldier aphids (Akimoto et al, 1996; Aoki & Kurosu, 2010).  These stay outside the gall and repel possible invaders.  It should thus not come as a surprise to find that in some species, the soldiers don’t just fight other aphids, but actually defend their siblings against predators, even being able to kill lacewing larvae (Kutsukake et al., 2004).

Truly a force to be reckoned with and of course why I love aphids so much.

Akimoto, S., Ozaki, K. &Matsumoto, Y. (1996). Production of first-instar defenders by the Hormaphidid gall-forming aphid Hamamelsites cristafoliae living anholocyclically on Betula maximowicziana. Japanese Journal of Entomology 64, 879-888.

Aoki, S. &Makino, S. (1982). Gall usurpation and lethal fighting among fundatrices of the aphid Epipemphigus niisimae. Kontyu 50, 365-376.

Aoki, S. & Kurosu, U. (2010) A review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche, 2010, http://connection.ebscohost.com/c/articles/60639059/

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

Kutsukake, M., Shibao, H., Nikoh, N., Morioka M., Tamura, T., Hoshino, T., Ohgiya, S, & Fukatsu, T. (2004) Venomous protease of aphid soldier for colony defense,  Proceedings of the National Academy of Sciences USA, 101,11338-11343. http://www.pnas.org/content/101/31/11338.full.pdf+html

Whitham, T. G. (1979). Territorial behaviour of Pemphigus gall aphids. Nature 279, 324-325.

http://www.nature.com/nature/journal/v279/n5711/abs/279324a0.html