Monthly Archives: June 2017

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

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.

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, and (right) Pemhigus bursarius gall (Photo Graham Calow

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

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

Pick and mix 7 – more eclectic links from the past week

Links to stuff I have read with interest; quite a lot about bees this week 😊

Interesting reflections on a life in science by Rich Lenski when he gave an address to newly graduated PhD students

A nice summary of what conservation biocontrol is all about, incidentally by a former PhD student of mine 🙂

An interesting opinion piece on how conservation efforts should move away from a species focus and use functional traits instead

Green walls – are they good for wildlife? – coincidentally written by another former student of mine 🙂

I totally agree – ecologists need to get outside more often

A blistering tale – what makes Blister beetles cause blisters

Saving the honeybee from the Varroa mite using a fungal biological control agent?

If you like bees and/or are a beekeeper, this interesting article by Norman Carreck, Science Director of the International Bee Research Association is a must read

Worrying evidence that it is not just insecticides that are killing bees – fungicides may also be a major culprit

On being a sustainable entomologist and helping to save the planet


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On Being Dead and a fictional ecology

Two very different books about fictional entomologists

I am ashamed to say, that until last summer, I had never heard of Jim Crace, let alone read anything by him.  Then my oldest friend (50 years since we first met at Ripon Grammar School) persuaded me that he was worth reading.   He was right, and I became hooked on Crace’s very distinctive style and diverse range of topics, ranging from the prehistoric to a dystopian future.  Then I came across Being Dead, which I at first thought was a murder mystery, but no, it turned out to be something completely different.  It is, in fact, a novel of many parts.  It is a retrospective view of the life of two entomologists who became matrimonially enjoined after they meet on a student expedition.  It is a love story with a difference. It is a commentary on bereavement and loneliness.  It is a story of life and death. I am however, not going to dwell on the plot, a fair bit of which describes the decomposition of the two bodies 🙂 Don’t be put off though, it is definitely a book worth reading.

Early on we are introduced to the study organisms of the two Doctors of Zoology, which is how Crace describes his two main characters*.  Celice works on the Oceanic Bladder Fly and Joseph on the Spray Hopper, Pseudogryllidus pelagicus. Crace’s description of the latter beast, a small (1 cm long) grey predatory beetle resembling a cricket, feeding on sea nits and sand lice at the ocean’s edge, was so cool, that, having never heard of this insect before, I was prompted to turn to the Great God Wikipedia, where, to my surprise, I found no mention of this fabulous beast!  Nor could I find it in Web of Science or Google Scholar.  I was forced to admit that I had been totally fooled and that the spray hopper was a figment, albeit very realistic, of Crace’s fertile imagination.   I am used to coming across ‘realistic’ fictional ecology in well-crafted science but have not often come across it in literary mainstream fiction so this was a bit of a surprise.

The Spray Hopper, Pseudogryllidus pelagicus, as imagined and very badly drawn by me

Being the nerd that I am, I went back to the start of the book and started reading it again, this time noting down every biological reference, checking these with Google, Google Scholar and Web of Science.  Luckily the spray hoper is mentioned fairly early on.

In addition to the already mentioned salt nits and sand lice, some other fictional insects appear, some with tantalising snippets of life cycle and habits.  These include the Polar cricket and Blind cave hoppers, which I assume are Orthopterans, three more beetle species, the Dune beetle, the Furnace beetle and Claudatus maximi a specialist herbivore, feeding on lissom grass. Three flies get a mention, Celice’s study organism, the Oceanic bladder fly which feeds on inshore wrack, the interestingly named Swag Fly, which seem to have a penchant for blood, and finally, the Sugar Flies, which as they are associated with fruit rind, I assume may be Drosophilids. There is a fleeting mention to the Squadron ant and an intriguing hemipteran, a flightless cicada, the Grease monkey, that feeds and breeds in diesel and is dispersed in the fuel tanks and engine blocks of trucks and lorries.

A number of birds are mentioned, but without much in the way of their biology, the only clues being in their names, Wood crow, Rock owls, Skin-eyed hawks  Sea jacks, Skimmers, Pickerling, and the  Hispid buzzard.   Crace almost slipped up with the latter, there is a Hispid hare, Caprolagus hipidus, also known as the Assam rabbit, which is native to south Asia.

Crace doesn’t just invent animals, he does plants as well.  Central to the decay theme and with several mentions is Festuca mollis or lissom grass.  Crace also gives us several alternative common names for this grass, angel bed, pintongue, sand hair, repose.  The adjectives he uses when talking about lissom grass are all indicative of its role in both the choice of location for the  act of sexual congress that unwittingly makes the entomological couple murder victims;  bed, mattress, irresistible, velvety, sensuous.  Again this is a totally made up species, although there is a Bromus mollis that depending on your source is either a synonym or a sub-species.

Then there are the wonderfully evocatively named plants, Flute bush, Sea thorn, the Tinder trees (described as being very dry), the Sea pine, also known as Slumber tree or Death’s Ladder, Vomitoria that grows in thickets, an imaginary relative of walnut,  Juglans suca that yields sapnuts, Stove weed with green bells, Pyrosia described as having high bracts, firesel, cordony and finally, the staple crop of the area, manac beans.

Three real plants get a mention, Spartina, red stem, Ammannia spp., which grows in water, and wet soil, and are used in aquariums and finally broom sedge Andropogon virginicus, native of the USA but a weed in Australia where it is known as whiskey grass as it was used as packaging for bottles of USA whiskey, which is a bit of trivia I didn’t know.

And finally, the one made up mammal, the Sea bat which given how few mammals there are, is entirely proper 🙂

All in all, reading Being Dead was a rewarding, if not entirely enjoyable experience, although I guess it depends on how you define enjoyable.  I do however, recommend it to you as good read, if only for the thrill of meeting the Spray hopper!

Coincidentally the next book I read was The Behaviour of Moths by Poppy Adams, which is also a murder story with an entomological connection, but unlike Being Dead, the entomology is hard core and totally real – I know, I checked J  Like Being Dead, it is also worth reading, although again, there are definitely metaphysical under- and overtones so ones enjoyment is tempered by having to think hard about what you are reading.

Read them back to back for the full experience and relax in the knowledge that you don’t need to keep fact checking as I have done it for you already 🙂


p* Strangely I was slightly irritated by this despite it reflecting that zoology, as I have always said, is mainly entomology 🙂



Filed under Book Reviews, EntoNotes

Pick and mix 6 – my top ten links from the past week

Some more links to follow, or not


An interesting article in Nature (makes a change) about the history of the peer review process

On the wondrous properties of spider silk and what we can use it for now and in the future

Using fake caterpillars to assess predation risk around the world

Speaking of fake, a spoof paper fooled a social science journal and two referees

On the value of Natural History Museums and why they should be preserved

On the importance of natural history training, although this is US-centric it is equally, if not more relevant to the UK as I have pointed out more than once

The Acrobatic Fly, a natural history (or should that be unnatural) film from 1910 – only three minutes so worth the time J

On broadening the western human diet to solve global food problems

How studying 25 000 dung beetles helped unravel the complexities of dung beetle evolution – great to see one of my former MSc students involved in this huge project

And to end with something completely different, a great post about what the charity Brass for Africa is doing for street children in Uganda through the medium of music teaching – I should add that my wife is one of the Trustees so I have a vested interest in advertising this 🙂


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