Tag Archives: aphids

Entomological classics – Aphids spit: visualising aphids feeding, the electrical penetration graph

Aphids as a taxonomic group, have been recognised since at least 1758 when Linnaeus coined the genus Aphis and have been cited as important pests for more than 200 years “The Aphis or Blighter, as we now for the first time venture to call it, from its being the most general cause of what are termed blights in plants..” (Curtis, 1802).  A detailed understanding of how they fed, was however, longer in being reached, but by 1914 the anatomy of the aphid mouthparts and the process of stylet insertion was fully described (Davidson, 1914).  Davidson (1923) also described the role that aphid saliva plays in helping the aphid feed by making it easier for the stylet to move between cells on its convoluted journey to the phloem, made visible as the so-called stylet tracks.

Drawings showing the effects produced by the passage of aphid stylets of three different aphid species through leaf tissue (Davidson, 1923).

Fast forward a couple of years and we have intrepid entomologists producing photographic evidence of aphid stylets in action (Smith, 1926).

Photomicrographs of the stylet of Myzus persicae in situ and the resultant stylet track (Smith, 1926).

One of the reasons that applied entomologists were so interested in aphid feeding was the role that aphids, and other insects, played as vectors of plant viruses, which until the 1920s, was not formally proven (e.g. Kunkel, 1926, Smith, 1926, 1929). You would be forgiven for thinking that once the connection between aphid feeding and plant virus transmission had been demonstrated then that would be it.  But no, much wants more, and aphidologists became intrigued about the link between aphid feeding and salivation, in particular when and exactly where these activities occurred in the plant.  Those entomologists working on plant viruses wanted to know which part of the feeding process was linked to the acquisition and inoculation of the viruses from and to the aphid host plant.  A possible solution to these conundrums, was, however, on the horizon.

In the early 1960s, two entomologists from the Department of Entomology, at the University of California, Davis, Donald McLean and Marvin Kinsey,  came up with a system that was to revolutionise the study of the feeding behaviour of aphids and other insects that feed internally on plant using piercing mouthparts (McLean & Kinsey, 1964). In essence, what they did was to make an aphid part of an electrical circuit by attaching a thin copper wire to its back using a quick-drying silver paint.  The feeding substrate, a leaf, had a 2.0 Volt, 60-cycle alternating current introduced to it and this was placed on an insulated grid connected to an amplifier connected in parallel with an oscilloscope, a chart-recorder and a speaker. The wire attached to the aphid, was joined to the grid and when the aphid began to feed this completed the circuit, and changes in voltage were able to be observed and recorded.  The next step was to identify which chart recordings were associated with sap ingestion and salivation by the aphid.  Using an artificial leaf, Parafilm stretched over a well containing a sucrose solution, and watching the aphids under a high power microscope, these innovative entomologists were able to identify four different stages involved in aphid feeding (Mclean & Kinsey, 1965).

The ground-breaking chart recording (Mclean & Kinsey, 1965) and as you might expect it was a pea aphid 🙂


A visual summary of what McLean and Kinsey were watching and recording (from Dixon (1973).

Not satisfied with these findings McLean and Kinsey modified their equipment and intensified their observations, sacrificing a number of aphids in the process.  When different waveforms were seen the poor aphids had their stylets amputated and the plant material with the stylet still in place was then examined under a high power microscope.  This meant that they were able to definitively correlate their recordings with the position of the stylet in different leaf tissues and during different behaviours (McLean & Kinsey, 1967).  As well as trying to understand how, when and where plant viruses were acquired or transmitted, it turns out that using the waveforms generated by the aphid mouthparts as they weave their way through the leaf tissues, is not only a useful way of assessing the resistance mechanism of a plant (e.g. Nielson & Don, 1974; Paul et al., 1996; ten Broeke et al., 2016) but also for detecting resistance to insecticides (e.g. Garzo et al., 2016).

Modifications to the original equipment happened very quickly; by 1966, a more compact and easier to use version using Direct Current had been developed (Schaefers, 1966). That said, the first correlation of a specific waveform and virus acquisition by the pea aphid, was shown using the original AC equipment (Hodges & Mclean, 1969).  A further modification of the Schaefers DC equipment was developed during the 1970s, such that test aphids were able to live and reproduce for up to ten days whilst attached to the set-up, thus allowing very detailed investigation of the correlations between the electrical signal patterns produced and the feeding behaviours of the aphids (Tjallingii, 1978).

Those of you who take note of such things, will have noticed, that so far, some 14-years after its invention, the term electrical penetration graph has not yet appeared, either here or in the scientific literature.   Earlier references to recordings using the technique use the term actograph which was somewhat non-specific, as it refers to any graphical representation of behavioural activity.  So when did the term Electrical Penetration Graph (EPG) first appear in the literature.  Google Scholar gave me a date of 1984 from a paper looking at the resistance of lettuce to the cabbage aphid Brevicoryne brassicae, a paper that includes Freddy Tjallingii in the authorship list (Mentink et al., 1984).  In this paper the authors refer to a conference proceedings paper (Tjallingii, 1982) as being the source of the name.  On tracking down that paper I found that it doesn’t actually mention the term EPG.  The first paper that specifically mentions and defines the term as “the recorded graph as a result of an overall electrical signal caused by stylet penetration activities” is Tjallingii (1985).  Strangely the author introduces the term thus “Here we introduce the term ‘electrical penetration graph (EPG)”, which I found slightly odd as it is a single author paper 😊  Inputting EPG or electrical penetration graph into Web of Science shows an increasing number of papers using and mentioning the technique, but surprisingly the first paper recorded is from 1999.

NGram finds the first mention slightly earlier, 1981.  A puzzle waiting to be solved for anyone with the time or inlcination.

The frequency of the occurrence of the phrase “Electrical penetration graph” according to Ngram Viewer (accessed and downloaded May 1st 2018).

The technique is now very well established and used around the world.  The equipment is commercially available through EPG Systems, which is where we got ours from and just in case you were wondering, this is what it looks like.

Faraday Cage (an earthed metal screen) surrounding the equipment to exclude electrostatic and electromagnetic influences

Our test plants in situ connected up to the electrical supply, recording equipment and amplifier.

Close up of the plants and EPG electrodes

Aphids connected up to the EPG. Photo courtesy of https://sites.google.com/site/ezwear1/epgIMG_0903.jpg

A simple guide to interpreting the waveforms


For Open Days and public displays it is not unknown for mischievous entomologists to link particular waveforms to recordings of sucking and spitting sounds and to play these back when the equipment is being demonstrated 🙂



Curtis, W.L. (1802) IV. Observations on aphides, chiefly intended to show that they are the principal cause of blights in plants, and the sole cause of the honeydewTransactions of the Linnaean Society of London, 6, 75-94.

Davidson, J. (1914) On the mouth-parts and mechanism of suction in Schizoneura lanigera, Hausmann. Zoological Journal of the Linnaean Society, 32, 307-330.

Davidson, J. (1923) Biological studies of Aphis rumicis Linn. The penetration of plant tissues and the source of the food supply of aphids.  Annals of Applied Biology, 15, 35-54.

Gabrys, B., Tjallingii, W.F. & van Beek, T.A. (1997) Analysis of EPG recorded probing by cabbage aphid on host plant parts with different glucosinolate contents. Journal of Chemical Ecology, 23, 1661-1673.

Garzo, E., Moreno, A., Hernando, S., Marino, V., Torne, M., Santamaria, E., Diaz, I. & Fereres, A. (2016) Electrical penetration graph technique as a tool to monitor the early stages of aphid resistance to insecticides. Pest Management Science, 72, 707-718.

Hodges, L.R. & McLean, D.L. (1969) Correlation of transmission of Bean Yellow Mosaic Virus with salivation activity of Acyrthosiphon pisum (Homoptera: Aphididae). Annals of the Entomological Society of America, 62, 1398-1401.

Kunkel, L.O. (1926) Studies on Aster Yellows. American Journal of Botany, 13, 646-705.

McLean, D.L. & Kinsey, M.G. (1964) A technique for electronically recording aphid feeding and salivation. Nature, 202, 1358-1359.

McLean, D.L. & Kinsey, M.G. (1965) Identification of electrically recorded curve patterns associated with aphid salivation and ingestion. Nature, 205, 1130-1131.

McLean, D.L. & Kinsey, M.G. (1967) Probing behavior of the pea aphid, Acyrthosiphon pisum. I. Definitive correlation of electronically recorded waveforms with aphid probing activitiesAnnals of the Entomological Society of America, 60, 400-405.

Mentink, P.J.M., Kimmins, F.M., Harrewijn , P., Dieleman, F.L., Tjallingii, W.F.,  van Rheenen, B. &  Eenink, A.H. (1984)  Electrical penetration graphs combined with stylet cutting in the study of host plant resistance to aphids. Entomologia experimentalis et applicata, 35, 210-213.

Nielson, M.W. & Don, H. (1974) Probing behaviour of biotypes of the spotted alfalfa aphid on resistant and susceptible and alfalfa clones.  Entomologia experimentalis et applicata, 17, 477-486.

Paul, T.A., Darby, P., Green, C.P., Hodgson, C.J. & Rossiter, J.T. (1996) Electrical penetration graphs of the damson-hop aphid, Phorodon humuli on resistant and susceptible hops (Humulus lupulus).  Entomologia expeimentalis et applicata, 80, 335-342.

Powell, G. (1991) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Annals of applied Biology, 119, 313-321.

Schaefers, G.A. (1966) The use of direct current for electronically recording aphid feeding and salivation. Annals of the Entomological Society of America, 59, 1022-1024.

ten Broeke, C.J.M., Dicke, M. & van Loon, J.J.A. (2016) Feeding behaviour and performance of Nasonovia ribisnigri on grafts, detached leaves, and leaf disks of resistant and susceptible lettuce.  Entomologia experimentalis et applicata, 159, 102-111.

Tjallingii, W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia experimentalis et applicata, 24, 521-530.

Tjallingii, W.F. (1982) Electrical recording of aphid penetration. [In] J.H. Visser & A.K. Minks (eds.) Proceedings of the 5th Symposium on Insect Plant-Relationships, 1-4 March, 1982, Wageningen, Pudoc, pp 409-410.

Tjallingii, W.F. (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia experimentalis et applicata, 38, 177-185.

Smith, K.M. (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plant. Annals of Applied Biology, 13, 109-139.

Smith, K.M. (1929) Studies on potato virus diseases, V. Insect transmission of potato leaf roll.  Annals of Applied Biology, 16, 209-229



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Not all aphids grow up to be aphids – the enemy within

It has been said that if aphids had their own way and unlimited resources the world as we know it would be 149 km deep in the cute little beasts (Harrington, 1994 ). Last year I wrote about how predators that feed on aphids, although useful, don’t really cut the mustard when it comes to keeping them in check and suggested that their host plants played a major role in keeping aphids from taking over the World.  While they do play an important part in keeping aphid populations under control, and are aided and abetted by aphid specific predators, there are, however, some much more efficient aphid-specific natural enemies out there.  They may be less conspicuous than the brightly coloured ladybirds that we often see munching their way through aphid colonies; public perception of their name may make people wince, but these beautiful and graceful creatures make sure that our appetite for salads and exotic vegetables out of season is satisfied safely and efficiently.  Their life cycles rival that of their prey, or should that be hosts, and entomologists fondly imagine that the film Alien was inspired by them 😊

I am, of course, talking about parasitic wasps, or parasitoids as they are more commonly known.  They are called parasitoids because unlike true parasites which generally speaking keep their hosts alive, insect victims of these wasps will, if successfully parasitized, die well before their non-parasitized relatives. In case you were wondering, the term parasitoid was coined by the Finnish Hemipterist, Odo Reuter (1913).  Aphids are not the only insects that are attacked by parasitoid wasps. The action of insect parasites has been known about for over two hundred years.  Erasmus Darwin, grandfather of the more famous Charles, noted that Ichneumonid wasps parasitised cabbage white butterfly caterpillars and so should be encouraged by gardeners (Darwin, 1800).  This is not the only early mention of parasitic insects in this context; Wheeler (1928), points out that back in the 1850s, two Italian entomologists, Camillo Rondani and Vittore Ghiliana also suggested the use of parasitic insects as biological control agents.  Aphid pests of glasshouse crops originally controlled mainly by predators (van Lenteren & Woets, 1988) are now routinely controlled by the application of commercially produced Braconid and Chalcid wasps (Boivin et al., 2012; van Lenteren, 2012).

Three commonly used aphid parasitoid biological control agents in action. Images from http://biologicalservices.com.au/products/aphelinus-2.html and https://www6.inra.fr/encyclopedie-pucerons/Especes/Parasitoides/Braconidae-Aphidiinae/Praon-volucre

When people think of Hymenoptera, they tend to think of bees, Vespid wasps and ants as being the most important and abundant.  They are very much mistaken.  The Parastica, or parasitoid wasps, are, by a huge margin, the most speciose and abundant section of

Parasitoids clearly dominate the Hymenopteran fauna of the British Isles (Many thanks to Natalie Dale-Skey of the NHM for permission to use this).

the Hymenoptera both in the UK and elsewhere

In the tropics the parasitoids are even more dominant. Data from Gaston et al., (1996).

Once parasitized, the egg(s), unless they are encapsulated by the aphid ‘immune’ system, hatch and begin to feed on the internal tissues of their, presumably, unsuspecting aphid host.  The parasitoid larvae avoid feeding on vital parts of the aphid, so that it can continue to grow and develop and provide food for the parasitoid, until the parasitoid is ready to pupate. Once the parasitoid is ready to pupate it delivers the coup de grace putting the aphid out of its misery and allowing the formation of the ‘mummy’ in

The three most common types of aphid mummies.  Images from http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavershttp://biologicalservices.com.au/products/aphelinus-2.html and https://farm1.static.flickr.com/327/18532751584_becc0e56e9_b.jpg respectively.

which the parasitoid completes its development before sawing its way out to emerge as a winged adult ready to seek out new hosts, leaving a characteristic neat circular hole in mummy case. In case you were wondering why the mummy of Praon volucre looks like it is sitting on a plate, this because, unlike the other aphid parasitoids, the final instar cuts its way out of the bottom of the aphid and spins its cocoon externally underneath the remnants of the aphid, hence the ‘plate’ (Beirne, 1942).

And out she comes; emerging parasitoid – http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers


Lysiphelbus testaceipes  Photo by J.K.Clark, University of California Statewide IPM Project

Once an aphid, now a hollow mummy; note the neat emergence holes.  Aphid parasitoids are very much tidier than the parasitic lifeform in the classic film Alien 🙂

Another aspect of their life style that makes parasitoids a breed apart from true parasites, is that as well as using aphids as egg laying sites for their larvae, the adults like to snack on them every now and then to help mature more eggs and to keep up their energy levels; sometimes quaintly described as predatism (Flanders, 1953).  Although the parasitoids can make feeding attacks at any time, they appear to feed first and then start laying their eggs (e.g. Collins et al., 1981).

Parasitoids are widely used as biological control agents in glasshouses and other protected environments as they are generally regarded as being more effective than predators (Debach & Rosen, 1991), although there is some support that generalist predators can play a significant part in biological control in the wider environment (Symondson et al., 2002; Gontijo et al., 2015).  That said, aphid parasitoids seem to be fairly host specific in that commercial companies offer specific parasitoid mixtures to control different aphid pest species e.g.  https://www.koppert.com/pests/aphids/product-against/aphipar/ [Note this is NOT an endorsement]. In fact it has been suggested that the relationship between aphids and their parasitoids can be used to clarify aphid taxonomic relationships (Mackauer, 1965). On the other hand, there are very few examples of monophagous aphid parasitoids, most being described as oligophagous (Stary & Rejmanek, 1981).   So given that there is a fair bit of evidence that the parasitoids attacking aphids do show some discrimination in their choice of hosts, how do they find them?

Parasitoids in general were originally thought to be “possessed of an unerring instinct that guided them in their search for hosts” but Cushman (1926) rebutted this idea pointing out that actually the parasitoids first home in on the habitat or food plant that their host lives in and then search for their host (Laing, 1937).   The parasitoids referred to by Cushman and Laing, are however, not parasitoids of aphids, attacking lepidopteran leaf miners and carrion feeding flies respectively, so you might perhaps think that aphid parasitoids could have a different strategy. Although habitat selection by parasitoids of lepidopteran larvae (Thorpe & Caudle, 1938) and sawfly larvae (Monteith, 1955), using olfactory cues of their host’s food plant was confirmed readily easily and early on, the situation with aphids was less clear cut. Manfred Mackauer for example, suggested that aphid parasitoids might be using visual cues, such as leaf deformities or damage to find their aphids hosts (Mackauer, 1965).  The breakthrough came when three cabbage loving entomologists from the USA used an olfactometer to first show that the Braconid parasitoid Diaeretiella rapae, responded positively to the odour of collards (what we in the UK call spring greens) and second to show a very strong preference for them to lay their eggs in the aphid Myzus persicae when it was feeding on crucifers rather than other host plants.  They attributed this to the presence of mustard oil, the chemical that gives cabbages their distinctive taste and suggested that once the aphid host plant was found then the parasitoids used visual cues to find their aphid victims (Read et al., 1970).  Six years later it was firmly established that parasitoids in general used olfactory cues both to locate the habitat of their host (long-range) and then a short-range to find and confirm the identity (contact chemicals) their insect hosts (Vinson, 1976).

It was thought that the aphid parasitoids were chemically ‘conditioned’ during their larval life within the aphid feeding on a host plant and that this influenced their adult host preferences (e.g. Sheehan & Shelton, 1989; Wickremasinghe & Van Emden, 1992).  These, and other similar results, seemed to support the Hopkins host selection principle (Hopkins, 1917) which states that adult preferences are learnt as larvae.  A very neat experiment by van Emden et al., (1996) proved this hypothesis wrong. They transferred aphid mummies from the plant on which they had been parasitized on to another host plant and this changed the preference of the emerging adult, seeming to suggest that this was how aphid parasitoids developed their host preferences.  Now comes the neat, and very tricky part; if however, the parasitoid pupae were removed (very carefully) from the mummy case and reared to adulthood in the absence of a host plant or mummy and kept in a glass tube, the emerging adults showed no preference for particular host plants, clearly showing that adult preferences were  not determined during larval development but ‘conditioned’ by exposure to the external skin of the aphid mummy on emergence (van Emden et al., 1996).  Using aphids reared on an artificial diet (Douloumpaka & van Emden, 2003) showed that the it was very likely that the mother parasitoid leaves a chemical cue in or around the egg(s) she lays and that this is later incorporated into the silk of the parasitoid pupa, thus inducing the host preference seen as an adult.

An additional twist to the story is that male and female parasitoids differ in their responses to odours.  Both sexes of Aphidius uzbekistanicus and A. ervi, parasitoids of cereal aphids in the UK, respond to plant odours, but only females respond to aphids (Powell & Zhi-Li, 1983).  Males of both species are, however, attracted to the odours of their respective females, suggesting the existence of a sex pheromone. The existence of a sex pheromone in aphid parasitoids had been suggested a few years earlier when it was shown that male D. rapae attempted to copulate with filter paper that had had female abdomens crushed on them (Askari & Alisha, 1979).  The existence of sex pheromones in aphid parasitoids has now been shown in several species (e.g. Decker et al., 1993; McNeil & Broduer, 1995).  Strangely, female parasitoids also respond to sex pheromones, but in their case, the sex pheromones of aphids.  It turns out that they ‘parasitise’ aphids in more than one way, they home in on their prey using the aphid sex pheromone and this enables them to find a suitable overwintering host (Hardie et al., 1991).  At other times of the year they also use other aphid indicators; several studies have shown that parasitoids use the presence of aphid honeydew to help them find their hosts (Budenberg, 1990; Bouchard & Cloutier, 1984; Gardner & Dixon, 1985).

Predators of aphids such as ladybirds use chemical markers to warn other ladybirds that they have laid eggs near aphid colonies, thus reducing the chances of cannibalism and competition (e.g. Oliver et al., 2006). Given that the eggs of aphid parasitoids are laid internally, they are in effect invisible, it would make sense if the parasitoids ‘marked’ their hosts in some way to avoid other parasitoids laying their eggs in an already parasitized aphid, superparasitism.  Sure enough, there is some evidence that some adult parasitoids can recognise aphids that already have larval parasitoids developing inside them although they don’t seem to be able to consistently recognise already parasitized aphids until some hours afterward (e.g. Cloutier et al., 1984).  In some cases, it seems that it is the aphid herself that prevents superparasitism by reacting more aggressively towards parasitoids after being attacked once (Gardner & Dixon, 1984) and also by the presence of dried siphuncular secretions on the aphid’s skin (Outreman et al., 2001).  The waxy secretion had an effect for up to a day or so after which the internal changes caused by the developing parasitoid larvae were enough to deter further oviposition attempts.

It is a good thing for the poor aphids that they have such a high reproductive rate, or they would truly be in dire straits.  On the other hand, as exemplified by the words of Jonathan Swift (1733),

“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em,
And so proceed ad infinitum

there are parasites of parasitoids, the hyperparasites, that help keep the numbers of parasitoids under control, and thus, indirectly, help aphids remain relatively abundant.



Askari, A. & Alisha, A. (1979) Courtship behavior and evidence for a sex pheromone in Diaeretiella rapae (Hymenoptera: Braconidae), the cabbage aphid primary parasitoid. Annals of the Entomological Society of America, 72, 79-750.

Beirne, B.P. (1942) Observations on the life-history of Praon volucre Haliday (Hym.: Braconidae), a parasite of the mealy plum aphis (Hyalopterus arundinis Fab.). Proceedings of the Royal Entomological Society of London, Series A, General Entomology, 17, 42-47.

Boivin, G., Hance, T. & Brodeur, J. (2012) Aphid parasitoids in biological control.  Canadian Journal of Plant Science, 92, 1-12.

Bouchard, Y. & Cloutier, C. (1984) Honeydew as a source of host-searching kairomones for the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae).  Canadian Journal of Zoology, 62, 1513-1520.

Budenberg, W.J. (1990) Honeydew as a contact kairomone for aphid parasitoidsEntomologia experimentalis et applicata, 55, 139-148.

Cloutier, C., Dohse, L.A. & Bauduin, F. (1984) Host discrimination in the aphid parasitoid Aphidius nigripes. Canadian Journal of Zoology, 62, 1367-1372.

Collins, M.D., Ward, S.A., & Dixon, A.F.G. (1981) Handling time and the functional response of Aphelinus thomsoni, a predator and parasite of the. Journal of Animal Ecology, 50, 479-487.

Cushman, R.A. (1926) Location of individual hosts versus systematic relation of hots species as a determining factor in parasitic attack. Proceedings of the Entomological Society of Washington, 28, 5-6.

Darwin, E. (1800) Phytologia: or The Philosophy of Agriculture and Gardening. P. Byrne, Grafton Street, London.

Debach, P. & Rosen, D. (1991) Biological Control by Natural Enemies, Cambridge University Press, New York.

Decker, U.M., Powell, W. & Clark, S.J. (1993) Sex pheromone in the cereal aphid parasitoids Praon volucre and Aphidius rhopalosiphiEntomologia experimentalis et applicata, 69, 33-39.

Douloumpaka, S. & van Emden, H.F. (2003) A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Mysuze persicae SulzerPhysiological Entomology, 28, 108-113.

Flanders, S.E. (1953) Predation by the adult Hymenopteran parasite and its role in biological control. Journal of Economic Entomology, 46, 541-544.

Gardner, S.M. & Dixon, A.F.G. (1984) Limitation of superparasitism by Aphidius rhopalosiphi: a consequence of aphid defensive behaviour. Ecological Entomology, 9, 149-155.

Gardner, S.M & Dixon, A.F.G. (1985) Plant structure and foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae).  Ecological Entomology, 10, 171-179.

Gaston, K.J., Gauld, I.D. & Hanson, P. (1996) The size and composition of the hymenopteran fauna of Costa Rica.  Journal of Biogeography, 23, 105-113.

Griffiths, D.C. (1960) The behaviour and specificity of Monoctonus paldum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigbi (Mosley) on lettuce. Bulletin of Entomological Research, 51, 303-319.

Hardie, J., Nottingham, S.F., Powell, W. & Wadhams, L.J. (1991) Synthetic aphid sex pheromone lures female parasitoids.  Entomologia experimentalis et applciata, 61, 97-99.

Harrington, R. (1994) Aphid layer. Antenna18, 50-51.

Hopkins, A.D. (1917) Contribution to discussion.  Journal of Economic Entomology, 10, 92-93.

Holler, C. (1991) Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments and sex pheromone specificities (Hymenoptera, Braconidae, Aphidiinae. Systematic Entomology, 16, 15-28.


Laing, J. (1937) Host-finding byinsect parasites 1. Observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescensJournal of Animal Ecology, 6, 298-317.

Mackauer, M. (1965) Parasitological data as an aid in aphid classification. Canadian Entomologist, 97, 1016-1024.

McNeil, J.N. & Brodeur, J. (1995) Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripesJournal of Chemical Ecology, 21, 959-972.

Monteith, L.G. (1955) Host preferences of Drino bohemica Mesn. (Diptera; Tachnidae) with particular reference to olfactory responses.  Canadian Entomologist, 87, 509-530.

Oliver, T.H., Timms, J.E.L., Taylor, A. & Leather, S.R. (2006) Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks. Bulletin of Entomological Research, 96, 25-34.

Outreman, Y., Le Ralec, A., Plantegenest, M., Chaubet, B, & Pierre, J.S. (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology, 47, 339-348.

Powell, W. & Zhi-Li, Z. (1983) The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants.  Physiological Entomology, 8, 439-443.

Reuter, O.M. (1913). Lebensgewohnheiten und Instinkte der Insekten (Berlin: Friendlander).

Stary, P. & Rejmanek, M. (1981) Number of parasitoids per host in different systematic groups of aphids: The implications for introduction strategy in biological control (Homoptera: Aphidoidea; Hymenoptera: Aphidiidae). Entomologica Scandinavica, Suppl. 15, 341-351.

Riley, W.A. (1931) Erasmus Darwin and the biologic* control of insects. Science, 73, 475-476.

Sheehan, W. & Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae).  Journal of Insect Behavior, 2, 743-759.

Symondson, W.O.C., Sunderland, K.D., & Greenstone, M.H. (2002) Can generalist predators be effective bicontrol agents? Annual Review of Entomology, 47, 561-594.

Thompson, W.R. (1930) The principles of biological control. Annals of Applied Biology, 17, 306-338.

Thorpe, W.H. & Caudle, H.B. (1938) A study of the olfactory responses of insect parasites to the food plant of their host.  Parasitology, 30, 523-528.

Van Emden, H.F., Spongal, B., Wagner, E., Baker, T., Ganguly, S. & Douloumpaka, S. (1996) Hopkins’ ‘host selection principle’, another nail in its coffin.  Physiological Entomology, 21, 325-328.

Van Lenteren, J.C. (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57, 1-20.

Van Lenteren, J.C. & Woets, J. (1988) Biological and integrated control in greenhouses.  Annual Review of Entomology, 33, 239-269.

Vinson, S.B. (1976) Host selection by insect parasitoids.  Annual Review of Entomology, 21, 109-133.

Wheeler, W.M. (1922). Social life among the insects: Lecture II. Wasps solitary and social. Scientific Monthly, 15, 68-88.

Wheeler, W.M. (1928) Foibles of Insects and Men.  Alfred Knopf, New York

Wickremasinghe, M.G.V. & Van Emden, H.F. (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology, 17, 207-304.

*This is how he spelt it; not a mistake on my part J


Filed under Aphidology, Aphids

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

Prunella – mistress of plasticity

Now that I have your attention, this is not an article about soft porn or fetishes, but rather a paean for that humble ‘weed’ Prunella vulgaris – Self-heal, Heal all, Woundwort, Heart of the Earth and many other names, depending on where in the World you come from.   Prunella vulgaris is in the family Lamiaceae, so related to mints and dead-nettles.  It is an edible weed, the young leaves can be used in salads and it can also be used in soups, stews, or used whole and boiled as a pot herb.

The instantly (to me at any rate) recognisable flower of Prunella vulgaris

Prunella as I will now familiarly call her, has a very wide geographical native range and has also been introduced into South America where she does very well indeed (Godoy et al., 2011).

Distribution of Prunella vulgaris, blue native, brown introduced. http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:455176-1

 The name Prunella is derived from ‘Brunella’, a word which is itself a derivative, coming from the German name for quinsy, (a type of throat inflammation), die Braüne, which it was historically used to cure.  That is the other aspect of this glorious plant, it has many medicinal properties, hence the many common names refer to its healing powers, almost as many as Athelas of Lord of the Rings fame 😊  It was traditionally used in European herbal medicine for sore throats, fever reduction and like Athelas, for accelerating the healing of wounds (Matthiolus, 1626).  More recently it has become of interest as a possible cure for conditions associated with the herpes simplex virus (Psotováa et al., 2003) and inhibiting anaphylactic shock and other immediate type allergic reactions (Shin et al., 2001).  So truly a wonder drug, and again proving that “Old Wives Tales” are in many cases based on more than just superstition.

My interest in Prunella vulgaris, is however, based on its wondrous plasticity, as the three photographs below show nicely.  Depending on grazing (or mowing) pressure, Prunella can grow to reproductive maturity at heights  ranging from just over 2 cm to just under 30 cm. Truly remarkable.

I am of course, not the first person to be fascinated by this plasticity and the taxonomic and evolutionary ins and outs of this lovely plant (Nelson, 1965; Warwick & Briggs, 1979) but I still find it fascinating, and who knows, perhaps one day I might do some work on it myself 😊

The other thing that I like about Prunella is that she is also provides a living for aphids.  She has her own rare and specific one, Aphis brunellae, but is also kind enough to let a few other species make a living on her, Aphis gossypii, Aphis nasturtiiAulacorthum solani,  Macrosiphum euphorbiae, the ubiquitous Myzus persicae, M. ornatus and Ovatomyzus chamaedrys (Blackman & Eastop, 2006).

Aphis brunellae, rare in the UK – with thanks to the two Bobs for permission to use the photograph. http://influentialpoints.com/Images/Aphis_brunellae_colony_on_Prunella_vulgaris_c2015-08-21_15-37-27ew.jpg


Finally, you will have noticed that the Prunella aphid is A. brunellae, which is derived from the original name of Prunella (I guess Prunella Scales is happy, she could have been Brunella Scales).  Interestingly, her alter-ego was not removed until fairly recently, her tombstone is shown below.


Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World’s Herbaceous Plants and Shrubs Volume 1 Host Lists and Keys.  Wiley, Oxford.

Godoy, O., Saldaña, A., Fuentes, N., Valladares, F. & Gianoli, E. (2011)  Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biological Invasions, 13, 1615-1625.

Matthiolus, P.A. (1626) Kräuterbuch.  Noringberg.

Nelson, A.P. (1965) Taxonomic and evolutionary implications of lawn races in Prunella vulgaris (Labiatae). Brittonia, 17, 160-174.

Psotová, J., Kolá, M., Sousek, J., Ívagera, Z., Vicar, J. &Ulrichová, J. (2003) Biological activities of Prunella vulgaris extract. Phytotherapy Research, 17, 1082-1087.

Shin, T.Y., Kim, Y.K. & Kim, H.M. (2001) inhibition of immediate-type allergic reactions by Prunella vulgaris in a murine model.  Immunopharmacology & Immunotoxicology, 23, 423–435.

Warwick, S.I. & Briggs, D. (1979) The genecology of lawn weeds III. Cultivation experiments with Achillea millefolium L., Bellis perennis L., Plantago lanceolata L., Plantago major L. and Prunella vulgaris L. collected from lawns and contrasting grassland habitats.  New Phytologist, 83, 509-536.



Filed under Science writing, Uncategorized

Pick and mix 9 – a few links to click

Links to things I thought might grab your fancy

Interested in plants?  Find the latest State of the World’s Plants report here

Butterfly lovers?  Special issue of Journal of Insect Conservation devoted to butterfly conservation

Communicating entomology through video

Speaking of which, I did one on aphids once upon a time 🙂

How bees see may help us develop better cameras

How bumblebee flight may help us develop better drones

The Sixth Mass Extinction of vertebrates on the way but what about all the invertebrates that keep the world functioning?

Interesting article on insect symbolism in 19th Century British art

Weirdly interesting art based on the “natural world” by Katie McCann

This account of sexism in academia shocked and horrified m

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Filed under Pick and mix

Not all aphid galls are the same

A galling experience – what on earth is an aphid-induced phytotoxemia?

Scientists, actually let me correct that, all members of specialist groups, be they plumbers or astrophysicists, love their jargon.  Insect-induced phytotoxemias is a great example. What entomologists and plant physiologists mean by this term is plant damage caused by an insect.  The visible damage that insects can cause to plants ranges from discolouration, lesions, and malformation of stems and leaves. As the title of this post suggests I am going to discuss galls.  Many insects produce galls, some of which can be spectacular such as Robin’s pin cushion gall caused by the wasp, Diplolepis rosae, but being a staunch aphidologist I am going to concentrate on various leaf deformities caused by aphids.

Robin’s pin cushion gall, caused by Diplolepis rosae.


Aphids are true bugs, they are characterised by the possession of piercing and sucking mouthparts, the stylets, think of a hypodermic needle, being the piercing part of the mouthparts.

Aphid mouthparts, showing the passage of the stylets to the phloem (Dixon, 1973).

It was originally thought that the various leaf deformities resulting from aphid feeding was a direct result of the mechanical damage caused by the stylet entering the leaf and rupturing cell walls or possibly by the transmission of a disease. A series of elegant experiments by Kenneth Smith in the 1920s showed however, that insect salivary gland extracts were needed to cause the damage (Smith, 1920, 1926).  Puncturing leaves with needles did not produce the same symptoms.  The leaf rolls, leaf curls and pseudo-galls caused by aphids vary between species even when the aphids are closely related or their host plants are.  As an example of the latter, the bird cherry-oat aphid, Rhopalosiphum padi, causes what I would describe as a leaf roll, i.e. the leaves curl in from the edges towards the mid-rib, to make something that resembles a sausage.

Leaf roll pseudo-galls on bird cherry, Prunus padus, caused by the bird cherry oat aphid, Rhopalosiphum padi.

On the other hand, the cherry blackfly, Myzus cerasi, that has Prunus avium as its primary host, causes what I describe as leaf curls (think ringlets and curls in human hair terms), in that the leaf rolls up from the tip down towards the stalk (petiole).

Leaf curl on Prunus avium caused by the Chery black fly, Myzus cerasi

Similarly, there are two closely related aphid species, Dysaphis devecta and D. plantaginea, both feed on apple leaves, but D. devecta prefers to feed on the smaller veins while D. plantaginea prefers to feed on the mid-rib. The former causes a leaf-roll, the latter a leaf curl.

Dysaphis galls http://influentialpoints.com/Gallery/Dysaphis_devecta_species_group_rosy_leaf-curling_apple_aphids.htm

As well as leaf rolls and leaf curls, some aphids are able to induce leaf folds.  The poplar-buttercup gall aphid, Thecabius affinis being a good example.

Leaf fold on poplar caused by Thecabius affinis Poplar-buttercup gall aphid. Photo from the excellent Influential Points web site. http://influentialpoints.com/Gallery/Thecabius_affinis_Poplar-buttercup_gall_aphid.htm

You might think that it is the aphid feeding site that causes the characteristic roll, curl or fold, but if groups of D. devecta or D. plantaginea are caged on the stem of an apple seedling, young leaves several centimetres away will develop leaf rolls characteristic of each species suggesting that they are caused by specific substances in the saliva of each aphid (Forrest & Dixon, 1975).  Aphid saliva is known to contain a huge range of proteins from amino acids to digestive enzymes (Miles, 1999) so it is highly likely that different aphid species have evolved different suites of enzymes that enable them exploit their respective host plants more efficiently.  Entomologists who work on plant galls suspect that there is something in the saliva that makes the plant’s hormones trigger the gall formation, but they freely admit that they are still just guessing.  Leaf rolls and curls are pretty tame when you come to look at the galls some aphids can induce.  Aphids from the family Pemphigidae cause structural deformations that totally enclose them and their offspring.

Petiole galls caused by (left) Pemphigus spyrothecae (photo Graham Calow, http://warehouse1.indicia.org.uk/upload/med-p1771un6n510nt146ugosslt1hip5.jpg) and (right) Pemhigus bursarius gall (Photo Graham Calow http://www.naturespot.org.uk/species/pemphigus-bursarius)

Pemphigus populitransversus, the Cabbage root aphid or poplar petiole aphid (Photo Ryan Gott Ryan Gott‏ @Entemnein)

Not all enclosed galls are on petioles, the witch-hazel cone gall aphid (Hormaphis hamamelidis causes very distinctive galls on the leaves of its host plant.

Cone galls on witch hazel caused by Hormapahis hamamelidis http://www.inaturalist.org/photos/377819

So what is it with insect galls?  Are they of any use?  Peter Price and colleagues (Price et al., 1987) very succinctly summarised the four hypotheses that address the adaptive value of insect galls; a) No adaptive value (Bequaert, 1924), b) adaptive value for the plant (Mani, 1964), c) adaptive value for plant and herbivore (mutual benefit) (Cockerell, 1890) and d) adaptive value for the insect.  This last hypothesis is further subdivided into nutritional improvements, micro-environmental improvements and natural enemy protection (Price et al., 1987).

Becquaert’s non-adaptive hypothesis is and was easily and quickly dismissed (Price et al., 1987), so I will move swiftly on to the plant-protection hypothesis which Price et al., dismiss almost as swiftly.  In essence if galls are not associated with enhanced growth and survival of the galled plant then there is no protection offered.  In fact, galling insects have been used as biological control agents against weeds (e.g. Holloway & Huffaker, 1953; Gayton & Miller, 2012) which to put it mildly, does not suggest any benefits accruing from being galled.  That said, you could argue (weakly) and assuming that the plant is in control of producing the gall, that by confining the insect to a particular part of the plant it is “contained” and can be dealt with if it is causing too much damage by for example premature leaf abscission (Williams & Whitham, 1986).

The mutual benefit hypothesis is also easily dismissed as there is no evidence that galls improve the fitness of a plant as galling insects are parasites of the plant.  You might argue that fig wasps and figs mutually benefit each other, but in this case I think we are looking at special case pleading as the fig wasp are pollinators (Janzen, 1979).

So that takes us on to the adaptive value for insects hypothesis which makes a lot more sense as it is the insect (in this case the aphid), that has made the investment in what you might justifiably term, mutagenic saliva (Miles, 1999).

There is overwhelming evidence so support the nutrition hypothesis that galled leaves and galls are nutritionally superior to ungalled leaves (Llewellyn, 1982); e.g. acting as nitrogen sinks (Paclt & Hässler, 1967; Koyama et al., 2004), enhancing development and fecundity for succeeding generations of aphids (e.g. Leather & Dixon, 1981) and providing better nutrition for non-galling aphids and other insects (e.g. Forrest, 1971; Koyama et al., 2004; Diamond et al., 2008).   I also found a description of an aphid, Aphis commensalis, the waxy buckthorn aphid, which lives in the vacated galls of the psyllid Trichochermes walker, but whether this is for protection or nutritional reasons is not clear (Stroyan, 1952). 

The microenvironment hypothesis which suggests that the galls provide protection from extremes in temperature and humidity was hard to support with published data when Price et al. (1987) reviewed the topic. They mainly relied on personal observations that suggested that this might be true.  I found only two references in my search (Miller et al, 2009) that supported this hypothesis, albeit one of which is for gall wasps.  I have so far only been able to find one reference that suggest galls benefit aphids, in this case protecting them from very high temperatures (Martinez, 2009).

The natural enemy protection hypothesis has been tested almost as much as the nutrition hypothesis and in general terms seems to be a non-starter as gall forming insects seem to be especially attractive to parasitoids; see Price et al., (1987) for a host of references.  Aphids, however, may be a different case, free-living aphids have many parasitoid species attacking them, but those aphids that induce closed galls are singularly parasitoid free, at least in North America (Price et al., 1987). Although this may have been from lack of looking, as parasitoids have been identified from galls of the aphid Pemphigus matsumarai in Japan (Takada et al., 2010).  Closed galls are not always entirely closed as some need holes to allow honeydew to escape and migrants to leave (Stone & Schonrogge, 2003) which can act as entry points for natural enemies, but cleverly, the aphids have soldier aphids to guard against such insect invaders.

Sometimes the potential predator can be a vertebrate.  The aphid Slavum wertheimae forms closed galls on wild pistachio trees, and are, as with many other closed gall formers, not attacked by parasitoids (Inbar et al., 2004).  Wild pistachios are, however, attractive food sources to mammalian herbivores and gall aphids being confined to a leaf, unlike free living aphids could be inadvertently eaten. The galls however, contain higher levels of terpenes than surrounding leaves and fruits and emit high levels of volatiles that deter feeding by goats and other generalist herbivores thus protecting their inhabitants (Rostás et al., 2013). Not only that, but to make sure that any likely vertebrate herbivores avoid their gall homes, they make them brightly coloured (Inbar et al., 2010).   Aphids really are great at manipulating plants.

Cauliflower gall on wild pistachio, caused by Slavum wertheimae (Rostás et al., 2013).

Leaf rolls and curls on the other hand are more open structures, and in my experience, aphids that form leaf rolls or curls, are very vulnerable once a predator finds them crowded together in huge numbers.  Gall-dwelling aphids, including those that live in rolls and curls, tend, however, to be very waxy, and this may deter the less voracious predators.  I tend to support the nutritional benefit hypothesis in that with host alternating aphids, the enhanced nutrition enables rapid growth and development and is a way of building up numbers quickly, and hopefully the aphids are able to migrate to a new host, before the natural enemies find them.

Real life drama, Rhopalosiphum padi on Prunus padus at Harper Adams University May-June 2017.  In this instance the aphids won, and the plant was covered in hungry ladybird larvae eating mainly each other and the few aphids that had not managed to reach adulthood.

One thing that struck me while researching this article was that all the aphids producing galls, rolls or curls were host-alternating species. A fairly easily tested hypothesis for someone with the time to review the biology of about 5000 aphids, is that only host alternating aphids go in for galls.  This could be a retirement job J.

There are, depending on which estimate you agree with, somewhere between 8 000 000 to 30 000 000 insect species (Erwin, 1982; Stork, 1993; Mora et al., 2011), but even the highest estimate suggests that only 211 000 of these are galling species (Espirito-Santos & Fernandes, 2007).  And a final thought, if galls are so great why don’t all aphids and other phloem and xylem feeding insects go in for them?


Becquaert, J. (1924) Galls that secret honeydew.  A contribution to the problem as to whether galls are altruistic adaptations.  Bulletin of the Brooklyn Entomological Society, 19, 101-124.

Cockerell, T.D.A. (1890) Galls. Nature, 41, 344.

Diamond, S.E., Blair, C.P. & Abrahamson, W.G. (2008) Testing the nutrition hypothesis for the adaptive nature of insect galls: does a non-adapted herbivore perform better in galls?  Ecological Entomology, 33, 385-393.

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

Erwin, T.L. (1982) Tropical forests: their richness in Coleoptera and other arthropod species. The Coleopterists Bulletin, 36, 74-75.

Espirito-Santos, M.M.  & Fernandes, G.W. (2007) How many species of gall-inducing insects are there on Earth, and where are they?  Annals of the Entomological Society of America, 100, 95-99.

Forrest, J.M.S. (1971) The growth of Aphis fabae as an indicator of the nutritional advantage of galling to the apple aphid Dysaphis devecta. Entomologia experimentalis et applicata, 14, 477-483.

Forrest, J.M.S. & Dixon, A.F.G. (1975) The induction of leaf-roll galls by the apple aphid Dysaphis devecta and D. plantagineaAnnals of Applied Biology, 81, 281-288.

Gayton, D. & Miller, V. (2012) Impact of biological control on two knapweed species in British Columbia. Journal of Ecosystems & Management, 13, 1-14.

Holloway, J.K. & Huffaker, C.B. (1953) Establishment of a root borer and a gall fly for control of klamath weed.  Journal of Economic Entomology, 46, 65-67.

Inbar, M., Wink, M. & Wool, D. (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on PistaciaMolecular Phylogenetics & Evolution, 32, 504-511.

Inbar, M., Izhaki, I., Koplovich, A., Lupo, I., Silanikove, N., Glasser, T., Gerchman, Y., Perevolotsky, A., & Lev-Yadun, S. (2010) Why do many galls have conspicuous colors?  A new hypothesis. Arthropod-Plant Interactions, 4, 1-6.

Janzen, D.H. (1979) How to be a fig. Annual Review of Ecology & Systematics, 10, 13-51.

Koyama, Y., Yao, I. & Akimoto, S.I. (2004) Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation.  Entomologia experimentalis et applicata, 113, 35-44.

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.

Llewellyn, M. (1982) The energy economy of fluid-feeding insects.  Pp 243-251, Proceedings of the 5th International Symposium on Insect-Plant Relationships, Wageningen, Pudoc, Wageningen.

Mani, M.S. (1964) The Ecology of Plant Galls. W Junk, The Hague.

Martinez, J.J.I. (2009) Temperature protection in galls induced by the aphid Baizongia pistaciae (Hemiptera: Pemphigidae).  Entomologia Generalis, 32, 93-96.

Miles, P.W. (1999) Aphid saliva.  Biological Reviews, 74, 41-85.

Miller, D.G., Ivey, C.T. & Shedd, J.D. (2009) Support for the microenvironment hypothesis for adaptive value of gall induction in the California gall wasp, Andricus quercuscalifornicus. Entomologia experientalis et aplicata, 132, 126-133.

Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., & Worm, B. (2011) How many species are there on earth and in the ocean? PloS Biology, 9(8):, e1001127.doi:10.1371/journal.pbio.1001127.

Paclt, J. & Hässler, J. (1967) Concentrations of nitrogen in some plant galls. Phyton, 12, 173-176.

Price, P.W., Fernandes, G.W. & Waring, G.L. (1987) Adaptive nature of insect galls.  Environmental Entomology, 16, 15-24.

Rostás, M., Maag, D., Ikegami, M. & Inbar, M. (2013) Gall volatiles defend aphids against a browsing mammal.  BMC Evolutionary Biology, 13:193.

Smith, K.M. (1920) Investigations of the nature and cause of the damage to plant tissue resulting from the feeding of capsid bugs.  Annals of Applied Biology,7, 40-55.

Smith, K.M. (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plantAnnals of Applied Biology, 13, 109-139.

Stone, G.N. & Schönrogge, K. (2003) The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18, 512-522.

Stork, N.E. (1993) How many species are there? Biodiversity & Conservation, 2, 215-232.

Stroyan, H.L.G. (1952) Three new species of British aphid.  Proceedings of the Royal Entomological Society B, 21, 117-130.

Takada, H., Kamijo, K. & Torikura, H. (2010) An aphidiine parasitoid Monoctonia vesicarii (Hymenoptera: Braconidae) and three chalcidoid hyperparasitoids of Pemphigus matsumurai (Homoptera: Aphididae) forming leaf galls on Populus maximowiczii in Japan.  Entomological Science, 13, 205-215.

Williams, A.G. & Whitham, T.G. (1986) Premature leaf abscission: an induced plant defense against aphids. Ecology, 67, 1619-1627.



Filed under Aphidology, Aphids

Data I am never going to publish – A tale of sixty trees

In 1981 I spent a lot of time trudging through snow, cross-country skiing and snow-shoeing my way across the snowy wastes of Finland to snip twigs off bird cherry trees.  This was part of my post-doc which was to develop a forecasting system for the bird cherry-oat aphid, Rhopalosiphum padi.  On returning to the lab I then spent many a happy hour counting how many aphid eggs were nestled in between the buds and the stem on each twig.  It was while doing this that I noticed that some of the twigs were infested with the overwintering larval shields of the bird cherry ermine moth, Yponomeuta evonymellus.  Of course I then started counting them as well 🙂  I noticed that trees with lots of aphid eggs didn’t have very many larval shields and I wondered why. Some later observations from marked trees in Scotland appeared to provide evidence that the aphids and the moths tended to either prefer different trees or perhaps excluded each other.

Negative correlation between moths and aphids – more moths equals fewer aphids and vice versa

Based on these data I hypothesised that the two insects were indirectly competing for resources by altering plant chemistry and/or architecture thus making the trees less or more suitable for egg laying in the autumn (Leather, 1988).  I tested this experimentally when I was working for the Forestry Commission in Scotland using potted bird cherry trees that I defoliated to a lesser or greater extent to see if I could induce changes in foliar quality and tree growth rates that might influence subsequent colonisation by the aphids and moths. As predicted, those trees that had been defoliated, albeit by me and not by moth larvae, were less attractive to aphids in the autumn (Leather, 1993).  These effects were still apparent five years after the beginning of the experiment (Leather, 1995) when I had to desert my trees as I moved to a new position at Imperial College’s Silwood Park campus.

Given that apart from the location, the SE of England, this was my idea of a dream job for life (colleagues at the time included John Lawton, Mike Hassell, Bob May, Stuart McNeill, Mike Way, Brad Hawkins, Shahid Naeem, Mike Hochberg, Chris Thomas to name but a few), I decided to start up two long-term projects to see me through the next 30 years, one observational (my 52 sycamore tree project), the other experimental, a follow up to my bird cherry defoliation experiment.

I went for a simplified design of my earlier experiments, just two defoliation regimes, one to mimic aphid infestation (50%), the other to mimic bird cherry ermine moth defoliation (100%) and of course a non-defoliated control.  I also planted the trees in the ground to better simulate reality.  Using potted plants is always a little suspect and I figured that I would need to do rather a lot of re-potting over the next 30 years 🙂

The grand plan!

I sourced my trees from a Forestry Commission nursery thinking that as the national organisation responsible for tree planting in the UK I could trust the provenance of the trees.  Things didn’t go well from the start.  Having planted my trees in autumn 1992 and established the treatments in the spring of 1993 I discovered that my bird cherry, rather than being from a native provenance (seed origin) were originally from Serbia! Hmm 🙂  It was too late to start again, so I decided to carry on.  After all, bird cherry although widely planted in the SE, has a native distribution somewhat further north and west, which meant I was already operating close to the edge of ‘real life’, so what did an extra 1600 kilometres matter?

The mainly ‘natural’ distribution of bird cherry (left, Leather, 1996) and the current distribution including ‘introduced’ trees https://www.brc.ac.uk/plantatlas/index.php?q=plant/prunus-padus

Next, I discovered that my fence was neither rabbit nor deer proof.  I almost gave up at this point, but having invested a lot of time and energy in setting up the plot I once again decided to carry on. On the plus side, the trees most heavily defoliated and bitten back were mainly from the 100% defoliation treatment, but did give me some negative growth rates in that year.

My original plan was to record height (annually), bird cherry egg numbers (every December), bird cherry ermine moth larval shields (annually), bud burst and leaf expansion once a week, leaf-fall (annually), and once a month, defoliation rates in two ways, number of damaged leaves and an overall estimation of percentage defoliation.  This was a personal project, so no grant funding and no funding for field assistants.  It soon became clear, especially when my teaching load grew, as Imperial started replacing whole organism biologists with theoretical and molecular biologists, and I was drafted in to take on more and more of the whole organism lecturing, that I would not be able to keep both of my long term projects going with the same intensity.  Given the ‘problems’, associated with the bird cherry project, I decided  that I would ditch some of my sampling, bud burst was scored on 21st March every year and defoliation only measured once, in late summer and egg sampling and height recording came to a halt once the trees grew above me (2005)!  This allowed me to carry on the sycamore project as originally intended*.

I kept an eye on the trees until I left Silwood Park in 2012, but by 2006 I was only monitoring bud burst and leaf fall feeling that this might be useful for showing changes in phenology in our ever-warming world.  One regret as I wandered between the then sizeable trees in the autumn of 2012 was that I had not taken a before and after photograph of the plots.  All I have are two poor quality photos, one from 2006, the other from 2012.

The Sixty Tree site April 2006.

The Sixty Tree site April 2010 with a very obvious browse line


So, after all the investment in time, and I guess to a certain extent money (the trees and the failed fencing, which both came out of my meagre start-up funding**), did anything worthwhile come out of the study?

The mean number of Rhopalosiphum padi eggs per 100 buds in relation to defoliation treatment

As a long-time fan of aphid overwintering it was pleasing to see that there was a significant difference not only between years (F= 8.9, d.f. = 9/29, P <0.001), but also between treatments with the trees in the control treatment having significantly more eggs laid on them than the 100% defoliation treatment (F= 9.9, d.f. = 2/ 29, P <0.001 with overall means of 1.62, 1.22 and 0.65 eggs/100 buds).  This also fitted in with the hypothesis that trees that are defoliated by chewing herbivores become less suitable for aphids (Leather, 1988).  I must admit that this was a huge surprise to me as I had thought that as all the trees were attacked by deer the year after the experimental treatments they would all respond similarly, which is why I almost gave up the experiment back in 1994.

Bud burst stage of Prunus padus at Silwood Park on March 21st 1996-2012; by treatment and combined

When it came to budburst there was no treatment effect, but there was a significant trend to earlier budburst as the trees became older which was strongly correlated with warmer springs, although as far as spring temperatures were concerned there was no significant increase with year.

Mean spring temperature (Silwood Park) 1993-2012 and relationship between mean spring temperature and bud bust stage on 21st March.

Mean date of final leaf fall of Prunus padus at Silwood Park 1995-2012; by treatment and combined

At the other end of the year, there was a significant difference between date of final leaf fall between years but no significant difference between treatments.  In retrospect I should have adopted another criterion.  My date for final leaf fall was when the last leaf fell from the tree.  Those of you who have watched leaves falling from trees will know that there are always a few who are reluctant to make that drop to the ground to become part of the recycling process.  Even though they are very obviously dead, they hang there until finally dislodged by the wind.   I should really have used a measure such as last leaf with any pigment remaining.  I am sure that if I could be bothered to hunt down the wind speed data I would find that some sort of correlation.

Mean height (cm) of Prunus padus trees at Silwood Park 1993-2005 and Diameter at Breast Height (DBH) (cm) at the end of 2012

Except for the year after the deer attack, the trees, as expected, grew taller year by year.  There was however, no significant difference between heights reached by 2005 or in DBH at the end of 2012 despite what looked like a widening gap between treatments.

Defoliation scores of Prunus padus at Silwood Park 1993-2004; % leaves damaged and overall defoliation estimates

My original hypothesis that trees that were heavily defoliated at the start of their life would be more susceptible to chewing insects in later life, was not supported.  There was no significant difference between treatments, although, not surprisingly, there was a significant difference between years.  Average defoliation as has been reported for other locations was about 10% (Kozlov et al., 2015; Lim et al., 2015).

Number of Prunus padus trees with severe deer damage

That said, when I looked at the severity of deer attack, there was no effect of year but there was a significant effect of treatment, those trees that had been 100% defoliated in 1993 being most attractive to deer.   In addition, 20% of those trees were dead by 2012 whereas no tree deaths occurred for the control and less severely defoliated treatments.

I confess to being somewhat surprised to find as many significant results as I did from this simple analysis and was momentarily tempted to do a more formal analysis and submit it to a journal.  Given, however, the number of confounding factors, I am pretty certain that I would be looking at an amateur natural history journal with very limited visibility.  Publishing it on my blog will almost certainly get it seen by many more people, and who knows may inspire someone to do something similar but better.

The other reason that I can’t be bothered to do a more formal analysis is that my earlier work on which this experiment was based has not really hit the big time, the four papers in question only accruing 30 cites between them.  Hardly earth shattering despite me thinking that it was a pretty cool idea;  insects from different feeding guilds competing by changing the architecture and or chemsitry of their host plant.  Oh well.  Did anything come out of my confounded experiment or was it a total waste of time?  The only thing published from the Sixty Trees was a result of a totally fortuitous encounter with Marco Archetti and his fascination with autumn colours (Archetti & Leather, 2005), the story of which I have related in a previous post, and which has, in marked contrast to the other papers, had much greater success in the citation stakes 🙂

And finally, if anyone does want to play with the data, I am very happy to give you access to the files.


Archetti, M. & Leather, S.R. (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus. Oikos, 110, 339-343. 50 cites

Kozlov, M.V., Lanta, V., Zverev, V., & Zvereva, E.L. (2015) Global patterns in background losses of woody plant foliage to insects. Global Ecology & Biogeography, 24, 1126-1135.

Leather, S.R. (1985) Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology, 10, 43-56.  14 cites

Leather, S.R. (1988) Consumers and plant fitness: coevolution or competition ? Oikos, 53, 285-288. 10 cites

Leather, S.R. (1993) Early season defoliation of bird cherry influences autumn colonization by the bird cherry aphid, Rhopalosiphum padi. Oikos, 66, 43-47. 11 cites

Leather, S.R. (1995) Medium term effects of early season defoliation on the colonisation of bird cherry (Prunus padus L.). European Journal of Entomology, 92, 623-631. 4 cites

Leather, S.R. (1996) Biological flora of the British Isles Prunus padus L. Journal of Ecology, 84, 125-132.  14 cites

Lim, J.Y., Fine, P.V.A., & Mittelbach, G.G. (2015) Assessing the latitudinal gradient in herbivory. Global Ecology & Biogeography, 24, 1106-1112.



*which you will be pleased to know, is being analysed as part of Vicki Senior’s PhD project, based at the University of Sheffield.

**£10 000 which even in 1992 was not overly-generous.


Filed under EntoNotes, Science writing, Uncategorized

Not all aphids are farmed by ants

One of the great things about working with aphids is that it gave me the chance to go back to my childhood entomological roots of playing with ants.  Most gardeners have had the experience when cruelly* running their finger and thumb down an aphid covered plant stem of finding their hand suddenly covered with ants.   As someone who has a very relaxed approach to aphids, I find the presence of ants on a plant a handy way of finding aphids, although sometimes the ants are there because of extra-floral nectaries.  So what exactly is going on when you find ants and aphids together?

It has long been known that some aphids are farmed or tended by some ant species.  According to Jones (1927) Goedart** was the first to describe the relationship scientifically (Goedart & Lister, 1685) and by the latter half of the 19th Century you can find illustrations such as the one below that appeared in Van Bruyssel’s fantastic foray into early science-communication.


An ant dairy maid coming to milk her aphids – their siphunculi and anuses are just visible if you look closely: cleverly made to look like cow heads (From Van Bruyssel, 1870)

The ant-aphid association is usually defined as a mutualism as the two species exist in a relationship in which each individual benefits from the activity of the other.  Just to confuse people however, the association is also sometimes termed trophobiosis*** (e.g. Oliver et al., 2008) which is a more symbiotic relationship.

The degree of dependence of the aphid on the ants varies from species to species.  Some aphids, especially those that live underground on plant roots, are unable to survive without their ant attendants (Pontin, 1978).   Pontin (1960) also reports seeing Lasius flavus workers licking aphid eggs which he suggests stops them from going mouldy as the licking removes fungal spores.  He also noted that those eggs that were not cared for in this way did not hatch.  Other aphids have a more facultative relationship, and are able to survive quite successfully without the help of their friendly neighbourhood ants.

We tend to think of aphids as soft squidgy defenceless things that are easy to squash.  To other insects however, they present a bit more of a challenge.  Aphids have structural and behavioural defences to keep them safe in the dangerous world of bug eat bug.  Alarm pheromones and dropping behaviour are commonly used by aphids to avoid meeting predators face to face (Dixon, 1958a).    Aphis also have a number of physical defences.  Their spihunculi (cornicles) can produce a quickly hardening wax to gum up ladybird jaws (Dixon, 1958b).  Other aphid species cover themselves with dense waxy coats that make them less palatable or accessible to natural enemies (Mueller et al., 1992).  Other aphids have thick skins (heavily sclerotized) and what entomologists term saltatorial leg modification; long legs to you and me, and so able to give a ladybird or other opportunistic insect predator a good kicking (Villagra et al., 2002).  These characteristics, which are all costly, are reduced or absent in aphids that are frequently associated with ants (Way, 1963) as presumably with ant bodyguards in attendance, there is no need for the aphids to invest in extra anti-predator defences.


Note also the shortened siphunculi in Periphyllus testudinaceus and the hairier bottom, when compared with the leggy, and arguably, prettier Drepanosihpum platanoidis.

Apart from reducing their defensive armoury, those aphids that are obligately ant attended have a specially adapted rear end, essentially a hairy bottom.  This is more scientifically known as the trophobiotic organ.   The trophobiotic organ is an enlarged anal plate surrounded by special hairs that acts as a collection and storage device that allows the aphid to accumulate honeydew ready for the ants to remove at their leisure.


Three different trophobiotic organs, some hairier than others – after Heie (1980)


A real live view of the “trophobiotic organ” of Tetraneura ulmi (from the fantastic Influential Points website – http://influentialpoints.com/Images/Tetraneura_ulmi_aptera_on_grass_roots_c2015-09-04_14-53-13ew.jpg

Non-ant attended aphids without the trophobiotic organ, deposit their honeydew directly on to the leaf surface or on the ground, or if you are unlucky enough to park under an aphid infested tree, on to your car 🙂  Ants lick and collect sycamore aphid, Drepanosiphum platanoidis honeydew from leaves, but not directly from the aphids, which they do do from the maple aphid, Periphyllus testudinaceus, which also lives on sycamore trees P. testudinaceus (Pontin, 1958).

So what’s in it for the ants?  Why should they bother looking after aphids, even in some cases, keeping aphid eggs in their nests over the winter (Pontin, 1960)? The obvious answer is the honeydew that the aphids produce as a by-product of feeding on phloem sap. The amount of material that an aphid can remove from a plant is quite astounding.  A large willow aphid (Tuberolacnhus salignus) adult can sucks up the equivalent of 4 mg sucrose per day Mittler (1958) , which is equivalent to the photosynthetic product of one to two leaves per day.  Admittedly, they are large aphids and not ant attended****, but even an aphid half their size passes a lot of plant sap through their digestive systems.  Honeydew is not just sugar but is a mixture of free amino acids and amides, proteins, mineral and B-vitamins, so all in all, quite a useful food source for the ants (Way, 1963).  All aphids produce honeydew but not all aphids are ant attended and as I pointed out earlier, not all ants attend aphids.  Our research suggests that 41% of ant genera have trophobiotic species, but these are not equally distributed among ant families.  Some ant sub-families, for example the Fomicinae,  specilaise in ant attendance,  whereas in other ant families such as the Ecitoninae, aphids are used only as prey and the honeydew is gathered from plant and ground surfaces (Oliver et al., 2008).  The ant species that are most likely to develop mutualistic relationship with aphids appear to be those that live in trees, have large colonies, are able to exploit disturbed habitats and are dominant or invasive species (Oliver et al., 2008).

Those ants that do tend aphids don’t just protect them from predators and other natural enemies. They want to maximise the return for their investment. The black bean aphid, Aphis fabae, which is often tended by Lasius niger, has its tendency to produced forms reduced by the ants, thus making sure that the aphids are around longer to provide food for them (El-Ziady & Kennedy, 1956).  The ant Lasius fuliginosus transports young Stomaphis quercus aphids to parts of the tree with the best honeydew production (Goidanich, 1959) and Lasius niger goes one step further, moving individuals of the aphid Pterocomma salicis, to better quality willow trees (Collins & Leather, 2002).  Lasius niger seems to have a propensity for moving bugs about, they have also been seen moving coccids from dying clover roots to nearby living ones (Hough, 1922).

In the mid-1970s John Whittaker and his student, Gary Skinner, set up a study to examine the interactions between the wood ant, Formica rufa and the various insect herbivores feeding on the sycamore trees in Cringlebarrow Wood, Lancashire.  They excluded some ants from some of the aphid infested branches and allowed them access to others on the same trees and also looked at trees that were foraged by ants and those that weren’t.  They found that F. rufa was a heavy predator of the sycamore aphid, D. platanoidis, but tended the maple aphid,  P. testudinaceus (a novel observation for that particular ant-aphid interaction).  Ant excluded colonies of P. testudinaceus decreased, whereas D. platanoidis did not, but on those branches where ants were able to access the aphids, the reverse pattern was seen (Skinner & Whittaker, 1981).

The presence of thriving aphid colonies in the neighbourhood of ant nests and in some cases aphid colonies only exist where there are ant nests nearby (Hopkins & Thacker, 1999), has made some people wonder if aphids actively look for ant partners (Fischer et al., 2015).  There is, however, no evidence that aphids look for ant partners, rather the fact that wing production is reduced in the presence of tending ants, means that aphid colonies can accumulate around and close to ant nests (Fischer et al., 2015a).

That doesn’t mean that the aphids only rely on honeydew production to guarantee the presence of their ant bodyguards. The aphid Stomaphis yanonis, which like other


Stomaphis aceris, also ant attended.  Imagine trying to drag that mouth part out of a tree trunk quickly 🙂

Stomaphis species, has giant mouthparts, and so needs plenty of time to remove its mouthparts safely definitely needs ant protection to cover its back when involved in the delicate operation of stylet unplugging. In this case, it turns out that the aphids smell like that ants, they have cuticular hydrocarbons that resemble those of their ant protector Lasius fuji and thus encourages the ants to treat them as their own (Endo & Itino (2013).  Earlier work on the ant-attended tree-dwelling aphids, Lachnus tropicalis and Myzocallis kuricola, in Japan showed that the ant Lasius niger preyed on aphids that had not been attended by nest mates, but tended those that had been previously tended (Sakata 1994).  This too would indicate the presence of some sort of chemical marker or brand.

To add support to this, just over twenty years ago (1996), I supervised an undergraduate student Arran Frood*****.   He worked with the maple aphid, and the ants L. niger and L. fulginosus.  Aphids on ant-attended sycamore trees were washed with diluted acetone or water.   Those that had been washed with acetone were predated more than unwashed aphids suggesting that It was like washing off the colony specific pheromone marker. In support of this hypothesis, Arran found that predation would also increase if he swapped a twig full of aphids between colonies, but not from one part of the colony to another. It also worked between the two ant species, Lasius niger and L. fuliginosus, so it seems like the ants have a colony specific marker on their aphids.  We should really have written this up for publication.

Although aphids do not actively seek ant partners, they may compete with each other to retain the services of their ant bodyguards by producing more honeydew (Addicott, 1978).  There is evidence that ants make their decisions of whether to predate or tend aphids by monitoring honeydew production and choose to prey on aphids in colonies that produce less honeydew (Sakata, 1995).  Recent work has also shown that the honeydew of the black bean aphid, Aphis fabae is often colonised by the bacterium Staphylococcus xylosus. Honeydew so infected produces a bouquet of volatile compounds that are attractive to the ant L. niger thus increasing the cahnces of the aphids being ant-attended (Fischer et al., 2015b).  This adds yet another layer of complexity to the already complicated mutualistic life style that aphids have adopted.

And finally, you may remember me writing about the wonderful colour variations seen in some aphid species and how this could be modified by their symbionts. In another twist, it seems that ants may have a say in this too, albeit at a colony level rather than at the clonal level.  The improbably named Mugwort aphid, Macrosiphoniella yomogicola  which is obligately ant-attended by the ant L. japonicus, is found in  colonies that are typically 65% green 35% red (Watanabe et al. 2016).  The question Watanabe and his colleagues asked is why do ants like this colour balance? One possibility is that red and green aphids have slightly different effects on the mugwort plants where they feed. Though green aphids produce more honeydew, red aphids seem to prevent the mugwort from flowering. Given that aphid colonies on a flowering mugwort go extinct, ants looking to maintain an aphid herd for more than a year might see an advantage to keeping reds around to guarantee a long-term food supply from their green sisters.

Aren’t insects wonderful?



Addicott, J.F. (1978) Competition for mutualists: aphids and ants.  Canadian Journal of Zoology, 56, 2093-2096.

Carroll, C.R. & Janzen, D.H. (1973) Ecology of foraging by ants.  Annual Review of Ecology & Systematics, 4, 231-257

Collins, C.M. & Leather, S.R. (2002) Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality?  Ecological Entomology, 27, 238-241.

Dixon, A.F.G. (1958a) 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. (1958b) The protective function of the siphunculi of the nettle aphid, Microlophium evansi (Theob.). Entomologist’s Monthly Magazine, 94, 8.

El-Ziady, S. & Kenendy, J.S. (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli.  Proceedings of the Royal Entomological Society London (A), 31, 61-65

Endo, S. & Itino, T. (2012) The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons.  Research on Population Ecology, 54, 405-410.

Endo, S. & Itino, T. (2013) Myrmecophilus aphids produce cuticular hydrocarbons that resemble those of their tending ants.  Population Ecology, 55, 27-34.

Fischer, C.Y., Vanderplanck, M., Lognay, G.C., Detrain, C. & Verheggen, F.J. (2015a) Do aphids actively search for ant partner?  Insect Science, 22, 283-288.

Fischer, C.Y., Lognay, G.C., Detrain, C., Heil, M., Sabri, A., Thonart, P., Haubruge, E., & Verheggen, F.J. (2015) Bacteria may enhance species-association in an ant-aphid mutualistic relationship. Chemoecology, 25, 223-232.

Goidanich, A.  (1959) Le migrazioni coatte mirmecogene dello Stomaphis quercus Linnaeus, afido olociciclio monoico omotopo. Bollettino dell’Istituto di Entomologia della Università degli Studi di Bologna, 23, 93-131.

Goedart, J. & Lister, M. (1685) De Insectis, in Methodum Redactus; cum Notularum Additione. [Metamorphosis Naturalis] Smith, London.

Heie, O. (1980)  The Aphdioidea (Hemiptera) of Fennoscandia and Denmark. 1. Fauna Entomologica Scandinavica 9.Scandinavian Science Press, Klampenborg, Denmark.

Hough, W.S (1922) Observations on two mealy bugs Trionymus tritolii Forbes and Pseudococcus maritimus Ehrh. Entomologist’s News, 33, 1 7 1-76.

Hopkins, G.W. & Thacker, J.I. (1999) Ants and habitat specificity in aphids. Journal of Insect Conservation, 3, 25-31.

Jones, C.R. (1927) Ants and Their Relation to Aphids.  PhD Thesis, Iowa State College, USA.

Mittler, T.E. (1958a) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae).  II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew.  Journal of Experimental Biology, 35, 74-84.

Mueller, T.F., Blommers, L.H.M. & Mols, P.J.M. (1992) Woolly apple aphid (Eriosoma lanigerum Hausm., Hom., Aphidae) parasitism by Aphelinus mali Hal. (Hym., Aphelinidae) in relation to host stage and host colony size, shape and location.  Journal of Applied Entomology, 114, 143-154.

Oliver, T.H., Leather, S.R. & Cook, J.M. (2008)  Macroevolutionary patterns in the origin of mutualisms,  Journal of Evolutionary Biology, 21, 1597-1608.

Pontin, A.J. (1958)  A preliminary note on the eating of aphids by ants of the genus Lasius. Entomologist’s Monthly Magazine, 94, 9-11.

Pontin, A.J. (1960)  Some records of predators and parasites adapted to attack aphids attended by ants.  Entomologist’s Monthly Magazine, 95, 154-155.

Pontin, A.J. (1960)  Observations on the keeping of aphid eggs by ants of the genus LasiusEntomologist’s Monthly Magazine, 96, 198-199.

Pontin, A.J. (1978) The numbers and distributions of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecological Entomology, 3, 203-207.

Sakata, H. (1994) How an ant decides to prey on or to attend aphids.  Research on Population Ecology, 36, 45-51.

Sakata, H. (1995) Density-dependent predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attendant aphids Lachnus tropicalis and Myzocallis kuricola (Homoptera: Aphidae). Research on Population Ecology, 37, 159-164.

Skinner, G.J. & Whittaker, J.B. (1981) An Experimental investigation of inter-relationships between the wood-ant (Formica rufa) and some tree-canopy herbivores.  Journal of Applied Ecology, 50, 313-326.

Stadler, B. & Dixon, A.F.G. (1999)  Ant attendance in aphids: why different degrees of myrmecophily? Ecological Entomology, 24, 363-369.

Van Bruyssel, E. (1870) The Population of an Old Pear Tree.  MacMillan & Co, London

Vilagra, C.A., Ramirez, C.C. & Niemeyer, H.M. (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state.  Animal Behaviour, 64, 677-683.

Watanabe, S., Murakami, T., Yoshimura, J. & Hasegawa, E. (2016) Color piolymorphism in an aphid is maintained by attending ants.  Science Advances, 2, e1600606

Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera.  Annual Review of Entomology, 3, 307-344.

*in my opinion at any rate 🙂

**I have had to take this on faith as have not been able to get hold of the original reference and read it myself

***Trophobiosis is a symbiotic association between organisms where food is obtained or provided. The provider of food in the association is referred to as a trophobiont. The name is derived from the Greek τροφή trophē, meaning “nourishment” and -βίωσις -biosis which is short for the English symbiosis

****Perhaps they are too big for ants to mess with?  They are, however, very often surrounded by Vespid wasps who do appreciate the huge amount of honeydew deposited on the willow leaves and stems.

***** He must have enjoyed it because he also did his MSc project with me the following year 🙂


Post script

I began this post with an illustration from Van Bruyssel.  I finish it with this illustration from another early attempt to get children interested in entomology.  Unfortunately in this case the  ant attended aphids are the very opposite of what they should look like and he further compounds his error by telling his youthful audience that the aphids milk the aphids via their siphunculi 😦


The very opposite of what an ant-attend aphid looks like – from Half hours in the tiny world; wonders of insect life by C.F. Holder (1905)

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Filed under Aphidology, Aphids

Insects in flight – whatever happened to the splatometer?

I have been musing about extinctions and shifting baselines for a while now; BREXIT and an article by Simon Barnes in the Sunday Times magazine (3rd September 2016) finally prompted me to actually put fingers to keyboard.  I fear that BREXIT will result in even more environmental damage than our successive governments have caused already.  They have done a pretty good job of ignoring environmental issues and scientific advice (badgers) even when ‘hindered’ by what they have considered restrictive European legislation and now that we head into BREXIT with a government not renowned for its care for the environment I become increasing fearful for the environment. Remember who it was who restructured English Nature into the now fairly toothless Natural England, because they didn’t like the advice they were being given and whose government was it who, rather than keep beaches up to Blue Flag standard decided to reclassify long-established resort beaches as not officially designated swimming beaches?  And, just to add this list of atrocities against the environment, we now see our precious ‘green belt’ being attacked.

My generation is liable to wax lyrical about the clouds of butterflies that surrounded us as we played very non PC cowboys and Indians outside with our friends in the glorious sunshine.  We can also fondly reminisce about the hordes of moths that used to commit suicide in the lamp fittings or beat fruitlessly against the sitting room windows at night.  The emptying of the lamp bowl was a weekly ceremony in our house.  We also remember, less fondly, having to earn our pocket-money by cleaning our father’s cars, laboriously scraping the smeared bodies of small flies from windscreens, headlamps and radiator grilles on a Saturday morning.  A few years later as students, those of us lucky enough to own a car, remember the hard to wash away red smears left by the eyes of countless Bibionid (St Mark’s) flies, as they crashed into our windscreens.


Typical Bibionid – note the red eyes; designed specially to make a mess on your windscreen 🙂 https://picasaweb.google.com/lh/photo/GBgoGHhRbj-eUUF9SxZ4s9MTjNZETYmyPJy0liipFm0?feat=embedwebsite

Are these memories real or are we looking back at the past through those rose-tinted glasses that only show the sunny days when we lounged on grassy banks listening to In the Summertime and blank out the days we were confined to the sitting room table playing board games?

We have reliable and robust long-term data sets showing the declines of butterflies and moths over the last half-century or so (Thomas, 2005; Fox, 2013) and stories about this worrying trend attract a lot of media attention. On a less scientific note, I certainly do not find myself sweeping up piles of dead moths from around bedside lamps or extricating them from the many spider webs that decorate our house.  Other charismatic groups, such as the dragonflies and damselflies are also in decline (Clausnitzer et al., 2009) as are the ubiquitous, and equally charismatic ground beetles (carabids) (Brooks et al., 2012).  But what about other insects, are they too on the way out?  A remarkable 42-year data set looking at the invertebrates found in cereal fields in southern England (Ewald et al., 2015) found that of the 26 invertebrate taxa studied less than half showed a decrease in abundance; e.g. spiders, Braconid parasitic wasps, carabid beetles, Tachyporus beetles, Enicmus (scavenger beetles), Cryptophagid fungus beetles, leaf mining flies (Agromyzids), Drosophila, Lonchopteridae (pointed wing flies), and surprisingly, or perhaps not, aphids.  The others showed no consistent patterns although bugs, excluding aphids, increased over the study period.  Cereal fields are of course not a natural habitat and are intensely managed, with various pesticides being applied, so are perhaps not likely to be the most biodiverse or representative habitats to be found in the UK.

But what about the car-smearing insects, the flies, aphids and other flying insects?  Have they declined as dramatically?  My first thought was that I certainly don’t ‘collect’ as many insects on my car as I used to, but is there any concrete evidence to support the idea of a decline in their abundance.  After all, there has been a big change in the shape of cars since the 1970s.


Top row – cars from 1970, including the classic Morris 1000 Traveller that my Dad owned and I had to wash on Saturdays.

Bottom row the cars of today, sleek rounded and all looking the same.


Cars were  much more angular then, than they are now, so perhaps the aerodynamics of today’s cars filter the insects away from the windscreen to safety? But how do you test that?  Then I remembered that the RSPB had once run a survey to address this very point.  Sure enough I found it on the internet, the Big Bug Count 2004, organised by the RSPB.  I was very surprised to find that it happened more than a decade ago, I hadn’t thought it was that long ago, but that is what age does to you 🙂


The “Splatometer” as designed by the RSPB

The idea, which was quite cool, was to get standardised counts of insect impacts on car number platesThe results were thought to be very low as the quote below shows, but on what evidence was this based?

“Using a cardboard counting-grid dubbed the “splatometer”, they recorded 324,814 “splats”, an average of only one squashed insect every five miles. In the summers of 30-odd years ago, car bonnets and windscreens would quickly become encrusted with tiny bodies.”  “Many people were astonished by how few insects they splatted,” the survey’s co-ordinator Richard Bashford, said.

Unfortunately despite the wide reporting in the press at the time, the RSPB did not repeat the exercise.  A great shame, as their Big Garden Birdwatch is very successful and gathers useful data.   So what scientific evidence do we have for a decline in these less charismatic insects?  Almost a hundred years ago, Bibionid flies were regarded as a major pest (Morris, 1921) and forty years ago it was possible to catch almost 70 000 adults in a four week period from one field in southern England (Darcy-Burt & Blackshaw, 1987).   Both these observations suggest that in the past Bibionids were very common.  It is still possible to pluck adult Bibionids out of the air (they are very slow, clumsy fliers) in Spring, but if asked I would definitely say that they are not as common as they were when I was a student.  But as Deming once said, “Without data, you’re just another person with an opinion.”  In the UK we are fortunate that a long-term source of insect data exists, courtesy of Rothamsted Research, the longest running agricultural research station in the world.  Data have been collected from a nationwide network of suction and light traps for more than 50 years (Storkey et al., 2016).   Most of the publications arising from the survey have tended to focus on aphids (Bell et al., 2015) and moths (Conrad et al., 2004), although the traps, do of course, catch many other types of insect (Knowler et al., 2016).  Fortuitously, since I was interested in the Bibionids I came across a paper that dealt with them, and other insects likely to make an impact on cars and splatometers (Shortall et al., 2009).  The only downside of their paper was that they only looked at data from four of the Rothamsted Suction Traps, all from the southern part of the UK, which was a little disappointing.


Location and results of the suction traps analysed by Shortall et al. (2009).

Only three of the trap showed downward trends in insect biomass over the 30 years (1973-2002) analysed of which only the Hereford trap showed a significant decline.  So we are really none the wiser; the two studies that focus on a wider range of insect groups (Shortall et al., 2009; Ewald et al., 2015) do not give us a clear indication of insect decline.   On the other hand, both studies are limited in their geographic coverage; we do not know how representative the results are of the whole country.

What a shame the RSPB stopped collecting ‘splatometer’ data, we would now have a half-decent time series on which to back-up or contradict our memories of those buzzing summers of the past.

Post script

After posting this I came across this paper based on Canadian research which shows that many pollinators, possibly billions are killed by vehicles every year.  This reduction in insect numbers and biomass has also been reported in Germany.


Bell, J.R., Alderson, L., Izera, D., Kruger, T., Parker, S., Pickup, J., Shortall, C.R., Taylor, M.S., Verrier, P. & Harrington, R. (2015) Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids.  Journal of Animal Ecology, 84, 21-34.

Brooks, D.R., Bater, J.E., Clark, S.J., Montoth, D.J., Andrews, C., Corbett, S.J., Beaumont, D.A., & Chapman, J.W. (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss of insect biodiversity. Journal of Applied Ecology, 49, 1009-1019.

Clausnitzer, V., Kalkman, V.J., Ram, M., Collen, B., Baillie, J.E.M., Bedjanic, M., Darwall, W.R.T., Dijkstra, K.D.B., Dow, R., Hawking, J., Karube, H., Malikova, E., Paulson, D., Schutte, K., Suhling, F., Villaneuva, R.J., von Ellenrieder, N. & Wilson, K. (2009)  Odonata enter the biodiversity crisis debate: the first global assessment of an insect group.  Biological Conservation, 142, 1864-1869.

Conrad, K.F., Woiwod, I.P., Parsons, M., Fox, R. & Warren, M.S. (2004) Long-term population trends in widespread British moths.  Journal of Insect Conservation, 8, 119-136.

Darcy-Burt, S. & Blackshaw, R.P. (1987) Effects of trap design on catches of grassland Bibionidae (Diptera: Nematocera).  Bulletin of Entomological Research, 77, 309-315.

Ewald, J., Wheatley, C.J., Aebsicher, N.J., Moreby, S.J., Duffield, S.J., Crick, H.Q.P., & Morecroft, M.B. (2015) Influences of extreme weather, climate and pesticide use on invertebrates in cereal fields over 42 years. Global Change Biology, 21, 3931-3950.

Fox, R. (2013) The decline of moths in Great Britain: a review of possible causes. Insect Conservation & Diversity, 6, 5-19.

Knowler, J.T., Flint, P.W.H., & Flint, S. (2016) Trichoptera (Caddisflies) caught by the Rothamsted Light Trap at Rowardennan, Loch Lomondside throughout 2009. The Glasgow Naturalist, 26, 35-42.

Morris, H.M. (1921)  The larval and pupal stages of the Bibionidae.  Bulletin of Entomological Research, 12, 221-232.

Shortall, C.R., Moore, A., Smith, E., Hall, M.J. Woiwod, I.P. & Harrington, R. (2009)  Long-term changes in the abundance of flying insects.  Insect Conservation & Diversity, 2, 251-260.

Storkey, J., MacDonald, A.J., Bell, J.R., Clark, I.M., Gregory, A.S., Hawkins, N. J., Hirsch, P.R., Todman, L.C. & Whitmore, A.P. (2016)  Chapter One – the unique contribution of Rothamsted to ecological research at large temporal scales Advances in Ecological Research, 55, 3-42.

Thomas, J.A. (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups.  Philosophical Transactions of the Royal Society B, 360, 339-357


Filed under EntoNotes, Uncategorized

Ideas I had and never followed up

“When I was younger, so much younger than before” I never needed any help to come up with ideas for research topics or papers.   When I was doing my PhD and later as a post-doc, I used to keep a note pad next to my bed so that when I woke up in the middle of night with an idea (which I often did) I could scribble it down and go back to sleep.  (These days sadly, it is my bladder and not ideas that wake me up in the wee small hours 🙂*)

On waking up properly, these ideas, if they still seemed sensible, would  move onto Stage 2, the literature search.  In those days, this was much more difficult than it is now, no Google Scholar or Web of Science then, instead you had to wade though the many hard-copy Abstract series and then get hard copies of the papers of interest.  Once in my hands, either via Inter-library loans or direct from the author, or even photocopied from the journal issue (we did have photocopiers in those days), the papers would be shoved into a handy see-through plastic folder (Stage 3).  Depending on how enthusiastic I was about the idea, I would then either mock-up a paper title page or put the folder in the ‘to deal with later’ pile (Stage 4).   Many of these eventually led on to Stage 5, experiments and published papers.  Others have languished in their folders for twenty or thirty years.

As part of my phased run up to retirement (2021), I have started farming out my long-term publishable (hopefully) data-sets to younger, more statistically astute colleagues and ‘publishing’ less robust, but possibly useful data on my blog site.  I have also, somewhat halfheartedly since the task is monumental, started to go through my old field and lab books that


A monumental collection of data.  The top right picture is my 20-year sycamore data set.  I estimate that there are about 7 million data points in it; of which to date only 1.6 million, give or take a million, are computerised.  I also have a ten-year bird cherry aphid data set from Scotland, waiting to go on the computer, any volunteers?

are not yet computerised.  Whilst doing this I came across some Stage 3 folders, which as you can see from the colour of the paper have languished for some time.


The Forgotten Nine


There were nine forgotten/dismissed proto-papers, the oldest of which, judging by the browning of the paper and my corresponding address, dates from the early 1980s, and is simply titled “What are the costs of reproduction?”.  This appears to have been inspired by a talk given by Graham Bell at a British Ecological Society, Mathematical Ecology Group meeting in 1983.  In case you are wondering, this was one of those meetings supposed to bring theorists and empiricists together.   It didn’t work, neither group felt able to talk to each other 🙂  The idea, inevitably based on aphid data, didn’t bear any fruit, although I do have this graph as a souvenir.  If anyone wants


In those days we used graph paper 🙂

 the data, do let me know.

Slightly later, we find the grandly titled, “Size and phylogeny – factors affecting covariation in the life history traits of aphids”.  This had apparently been worked up from an earlier version of a paper, less grandly, but no less ponderously, titled, “Size and weight: factors affecting the level of reproductive investment in aphids”.  This is based on some basic dissection data from eight aphid species and presents the relationships, or lack of, between adult weight (or surrogate measure), ovariole number, potential fecundity and the number of pigmented embryos.  As far as I can remember these are data that Paul Wellings** and I collected as a follow-up to work we had published from a side project when we were doing our PhDs at the University of East Anglia (Wellings et al., 1980).  The second title was inspired by a paper by Stephen Stearns (Stearns, 1984), who was something of a hero of mine at the time, and was, I guess, an attempt to publish pretty simple data somewhere classier than it deserved 🙂  So this one seems to be a Stage 4, almost Stage 5 idea, and may, if I have time or someone volunteers, actually get published, although I suspect it may only make it to a very minor journal under its original title.

Then we have a real oddity, “Aphids, elephants and oaks: life history strategies re-examined”.  This one as far as I remember, is based on an idea that I had about r- and k-selection being looked at from a human point of view and not the organism’s point of view.  My thesis was that an oak tree was actually r-selected as over its life-time it was more fecund than an aphid 🙂  I suspect this was going to be aimed at the Forum section of Oikos.

The next one, dates from the late-1980s, “Protandry versus protogyny: patterns of occurrence within the Lepidoptera”, and reflects the fact that females of the pine beauty moth, Panolis flammea, on which I was then working, emerge before the males (Leather & Barbour, 1983; Leather, 1984), something not often reported in Lepidoptera.  I wondered what advantage (if any) this gave P. flammea.  I planned this one as a review or forum type paper but never got beyond the title and collecting two references (Robertson, 1987; Zonneveld & Metz, 1991).  I still think this is an interesting idea, but do feel free to have a go yourselves, as again, I suspect that I won’t actually get round to it.

Finishing off my time in Scotland, is a paper simply entitled, “Egg hatch in the bird cherry aphid, Rhopalosiphum padi.” I have ten years of egg hatch data from eight trees waiting to be analysed.  This is almost certainly not worth more than a short note unless I (or a willing volunteer) tie it in with the ten years data on spring and autumn populations on the same trees 🙂 Aphid egg data although not very abundant, is probably not in great demand.  My first published paper (Leather, 1980) was about egg mortality in the bird cherry aphid and 36 years later has only managed to accrue 32 citations, so I guess not an area where one is likely to become famous 🙂

I then have four papers dating from my time as an Associate Member of the NERC Centre for Population Biology at Silwood Park.   The first is titled, “The suitability of British Prunus species as insect host plants” and was definitely inspired by my foray into counting host plant dots as exemplified by the late great Richard Southwood (Leather, 1985, 1986).  I think I was going to look at palatability measures of some sort.

The next is called ‘Realising their full potential: is it important and how many insects achieve it?”  I’m guessing that this was a sort of follow-up to my second most-cited paper ever (Leather, 1988), the story of which you can read here, if at all interested.  Most insects, even those that are pests, die before achieving anywhere near their full reproductive potential, but then so do we humans, and our population continues to grow.  So in answer to the question, I guess not and no it doesn’t matter 🙂

Also linked to insect reproduction is the next paper, which I have followed up with the help of a PhD student, and do hope to submit in the near future, “Queue positions, do they matter”.  As this one may actually see the light of day, I won’t say anything further about it.

And finally, another one about aphid eggs, “Bud burst and egg hatch synchrony in aphids”.  This one was going to be based on my then ten-year sycamore aphid data but is now based on my twenty-year data set and is now in the very capable hands of a PhD student and hopefully will see the light of day next year.

There are also a number of other folders with no titles that are just full of collections of reprints.  I can only guess at what these ideas were so won’t burden you with them.

I mentioned at the beginning of this piece that I don’t wake up in the middle of the night with ideas any more.  As we get older I think there is a tendency to worry that we might run out of ideas, especially when, as we do in the UK, suffer from ludicrously underfunded research councils with very high rejection rates that don’t allow you to resubmit failed grant applications.  It was thus reassuring to see this recent paper that suggests that all is not lost after you hit the grand old age of 30.  That said, I do believe that as you move away from the bench or field, the opportunity to be struck by what you see, does inevitably reduce.  As a PhD student and post-doc you are busy doing whatever it is you do, in my case as an ecological entomologist, counting things, and inevitably you see other things going on within and around your study system, that spark off other ideas.  It was the fear of losing these opportunities as I moved up the academic ladder, which inevitably means, less field and bench time and more time writing grant applications and sitting on committees, that I specifically set aside Monday mornings (very early mornings) to my bird cherry plots and even earlier Thursday mornings to survey my sycamore trees.   Without those sacrosanct mornings I am pretty certain I would have totally lost sight of what is humanly possible to do as a PhD student or post-doc.  This, thankfully for my research group, means that I had, and have, realistic expectations of what their output should be, thus reducing stress levels all round.   As a side benefit I got to go out in the fresh air at least twice a week and do some exercise and at the same time see the wonderful things that were going on around and about my study areas and as a bonus had the chance to get some new ideas.



Leather, S.R. (1984) Factors affecting pupal survival and eclosion in the pine beauty moth, Panolis flammea (D&S). Oecologia, 63, 75-79.

Leather, S.R. (1985) Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology, 10, 43-56.

Leather, S.R. (1986) Insect species richness of the British Rosaceae: the importance of host range, plant architecture, age of establishment, taxonomic isolation and species-area relationships. Journal of Animal Ecology, 55, 841-860.

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. & Barbour, D.A. (1983) The effect of temperature on the emergence of pine beauty moth, Panolis flammea Schiff. Zeitschrift fur Angewandte Entomologie, 96, 445-448.

Robertson, H.G. (1987) Oviposition and site selection in Cactoblastis cactorum (Lepidoptera): constraints and compromises. Oecologia, 73, 601-608.

Stearns, S.C. (1984) The effects of size and phylogeny on patterns of covariation inthe life history traits of lizards and snakes. American Naturalist, 123, 56-72.

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.

Zonneveld, C. & Metz, J.A.J. (1991) Models on butterfly protandry – virgin females are at risk to die. Theoretical  Population Biology, 40, 308-321.


*I hasten to add that I do still have new ideas, they just don’t seem to wake me up any more 🙂

**Now Vice-Chancellor of the University of Wollongong



Filed under Science writing, Uncategorized