Tag Archives: Diplolepis rosae

Large, complex, beautiful and multi-chambered – Robin’s pincushion, rose bedeguar gall, mossy rose gall

As I wrote a little while ago, thanks to the Covid-19 lockdown I have been roaming the countryside around my rural retreat a lot more than I normally do. One of the things that I have noticed is that there seem to be a lot more of the spectacular galls caused by the gall wasp, Diplolepis rosae, than I can remember seeing in previous years. I have absolutely no empirical evidence for this observation, so it could all be down to shifting baselines (Jones et al., 2020). Nevertheless, to me they have been much more noticeable this year, perhaps confounding the insect apocalypse narrative (Leather, 2018), but then again, perhaps not.

I am, when it comes to galls, more of an expert on those caused by aphids, than on those induced by Hymenoptera, although, as it happens I am a co-author on an oak gall wasp paper (Walker et al., 2002).  Of course, that does not make me an expert. One the rose bushes in our front garden always has at least one of Robin’s spectacular pincushions clamouring for attention.  The others rarely have one and I have idly wondered about the host preferences of the wasp and the suitability of different roses for the development of the larvae.

Our front garden Diplolepis rosae gall

Having noticed that despite the relative abundance of the galls in the hedgerow roses, some bushes were totally gall-free while others supported several, sometimes in close proximity to each other, my thoughts immediately turned to possible student project.

Multiple infestations of Diplolepis rosae on hedgerow roses in the environs of Sutton, Staffordshire

A preliminary bit of research with the aid of Google Scholar quickly disabused me of that idea, but, as is the way with the internet, soon had me delving deep into the past in search of the history of this fascinating manifestation of insect activity.

My first discovery was that is also known as the rose bedeguar gall, something that had, until now, totally passed me by. According to my favourite dictionary (Gordh & Headrich, 2001),

“Bedeguar, Bedegar or Bedequar’ comes from a French word, bédégar, and is ultimately from the Persian, bād-āwar, meaning ‘wind-brought’”.

I’m guessing this meant that the first people to see them had no idea what caused them.

Not just complex galls

My next discovery was that D. rosae and the parasitoids that share its gall is a fairly well studied system (Randolph, 2005; Urban, 2018), although I am sure that it would still be possible to come up with some sort of project.  Diploelpis rosae is a member of the order Hymenoptera, so related to the larger and much more obvious bees, wasps and ants. It belongs to a family of wasps, the Cynipidae, commonly known as gall wasps.  Considering how small they are, 3.8 mm (Urban, 2018), the galls they make are spectacularly huge as are those that their relatives on oak form. Interestingly* more than 80% of gall wasps are associated with oaks, with most of the rest forming galls on members of the rose family (Shorthouse, 1973).  That in itself is, at least to me, an interesting fact; why such a restricted host range?  It is univoltine (one generation a year), overwinters as mature larva or pre-pupa in the galls, and emerges as adults in the spring when it seeks out suitable egg-laying sites. It is mainly parthenogenetic, although males are occasionally found (Callan, 1940; Stille, 1984). Despite being tiny, each wasp has the potential to lay about 500 eggs (Stille & Dävring, 1980). The adults are not very adventurous, usually laying eggs in the developing buds or flowers of the bush they emerged on, or on another close by (Bronner, 1985: Urban, 2018). That said, there must be some sort of host preference and selection going on, as in Sweden and the Czech Republic most galls are found on Rosa canina (Stille, 1984; Urban 2018). They also seem to favour younger bushes, or those that produce long vigorous stems (Stille, 1984).  The potentially high fecundity is presumably an adaptation to the high rates of parasitism that the larvae of D. rosae can experience, up to 70% in some cases (Stille, 1984).  In fact, so varied and numerous are the parasites, that many of the early papers about D. rosae pay more attention to the other inhabitants of the galls than they do the architects (Osten Sacken, 1870; Blair, 1945; Bugbee, 1951).  Females that lay a lot of eggs in the same developing bud produce bigger galls and a greater proportion of the larvae survive (Stille, 1984).

Survival of D. rosae in relation to gall weight (after Stille, 1984)

 It also appears that the closer to the ground the galls are, the lower the parasitism rate (Laszló, 2001).

The ideal strategy would then be for female D. rosae to lay big galls as low down on the plants as possible, but from personal observation this is not always the case , so as is often the case with the “Mother knows best” hypothesis there is something we humans are missing that the insects aren’t (Awmack & Leather, 2002).

Those darned taxonomists!

So, as so much is already known about this tiny wasp and its spectacular gall, I thought I would do a little bit of entomological archaeology and trace the entomological history of this little insect. Now I think taxonomists are wonderful people and have a huge respect for the very often unacknowledged work that they do, and am a great supporter of the campaign to make sure that people cite them in their papers (Packer et al., 2018), but they are a contentious bunch :-).  I mention this because inputting Diplolepis rosae into Google Scholar didn’t get me very far back in time, 1951 to be precise (Bugbee, 1951).  This paper justifies my good-natured jibe at the argumentative nature of taxonomists as he explains his renaming of what was then Rhodites rosae, by citing a 1917 paper (Rohwer & Fagan, 1917) who argued that the French entomologist Étienne Geoffroy (1725-1810) who raised the Genus Diplolepis in 1762, should take precedence over Theodor Hartig’s (1805-1880) 1840 Genus Rhodites. This pointed me back to the 1940s and the discovery that the mossy rose gall was then known as Rhodites rosae and I quote “I have recently published an epitome of  my own experience e in rearing from galls of R. rosae” (Blair, 1945). A bit more delving and I found that in France in the 1930s and in the USA in the 1920s, it was still known as R. rosae (Weld, 1926; da Silva  Tavares, 1930). Wending my back via citations I arrived in 1903 to find it listed as Cynips rosae (Ashmead, 1903).

Historical insights – Monsieur Wirey was ahead of his time

Armed with this knowledge, my journey back into the history of D. roase was much simplified and introduced me to a gem of a book, Insect Architecture by James Rennie  (1787-1867) (Rennie, 1851). Here I found an interesting account of galls in general but a detailed exposition of the Bedeguar gall of rose as he described it, including this rather nice drawing.

Professor Rennie presents some hypotheses on the formation of insect galls in general;

Many of the processes which we have detailed bear some resemblance to our own operations of building with materials cemented together; but we shall now turn our attention to a class of insect-architects, and who cannot, so far as we know, be matched in prospective skill by any of the higher orders of animals. We refer to the numerous family which have received the name of gall-flies,

  1. Wirey says, the gall tubercle is produced by irritation, in the same way as an inflamed tumor in an animal body, by the swelling of the cellular tissue and the flow of liquid matter, which changes the organization, and alters the natural external form. This seems to be the received doctrine at present in France. “

As you can see from the above he has little time for the French explanation (typical English exceptionalism) and puts forward his own idea that the galls are formed because the egg laying process blocks the vessels of the plant and the fluid that would normally flow unimpeded blows up the tissue surrounding the egg like a balloon.  Of course he was wrong and M. Wirey was correct :-).  Considering that he had no access to the sophisticated techniques we have he pretty much hit the nail on the head.

That aside, his book introduced me to an entomologist I had never heard of, Priscilla Wakefield (1751-1832), yet another overlooked and forgotten female scientist.

Possible projects?

Although my plans for lots of great MSc projects were reduced somewhat I have had a lot of educational fun and I think that there are still some things that could usefully be looked at, long term recording across multiple sites which I hope the British Plant Gall Society is doing would be interesting.  On my walks I noticed a lot of variability in size and phenology of gall formation.  At the end of August I was coming across small very fresh looking galls at the same time as I was seeing larger more advanced galls.

A very fresh looking Bedeguar gall, August 26th 2020, Sutton

As far as I can tell, the timing of gall formation and its effect on final size of the galls has not been looked at in detail; do early galls enter winter larger than later formed galls, or is it entirely due to the number of eggs laid?  Given the huge number of other inhabitants of the galls, at least fourteen different species (Laszló, 2001, there is probably a viable project in looking at the timing of invasion by the different gall parasites and the outcome this may or may not have on the final composition of the gall fauna.

Feel free to suggest additional projects in the comments.

References

Ashmead, W.H. (1903) Classification of the gall-wasps and the parasitic cynipoids, or the superfamily Cynipoidea. IV, Psyche, 10, 210-216.

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

Blair, K.G. (1945) Notes on the economy of the rose‐galls formed by Rhodites (Hymenoptera, Cynipidae). Proceedings of the Royal Entomological Society, Series A, 20, 26-31.

Bronner, R. (1985) Anatomy of the ovipositor and oviposition behavior of the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae). Canadian Entomologist, 117, 849-858.

Bugbee, R. E. (1951). New and described parasites of the genus Eurytoma illiger from rose galls caused by species of the cynipid genus Diplolepis Geoffrey Hymenoptera: Eurytomidae). Annals of the Entomological Society of America, 44, 213–261

Callan, E.Mc. (1940) On the occurrence of males of Rhodites rosae (l.) (Hymenoptera, Cynipidae). Proceedings of the Royal Entomological Society of London, Series A., 15, 21-26.

Da Silva Tavares, J. (1930) Quelques Cécidies du Centre de la France, Publications de la Société Linnéenne de Lyon75, 145-167.

Gordh, G & Headrick, D.H. (2001) A Dictionary of Entomology, CABI, Wallingford

Jones, L.P., Turvey, S.T.,  Massimino, D. & Papworth, S. K.(2020) Investigating the implications of shifting baseline syndrome on conservation. People & Nature,

Laszló, Z. (2001) The parasitic complex of Diplolepis rosae (LinnaeuS, 1758) (Hymenoptera, Cynipidae): influencing factors and interspecific relationships. Entomologica Romanica, 6, 133–140.

Leather, S.R. (2018) “Ecological Armageddon” – more evidence for the drastic decline in insect numbers. Annals of Applied Biology, 172, 1-3.

Osten Sacken, R. (1870) Contributions to the natural hstory of the Cynipidæ of the United State and their galls.  Transactions of the American Entomological Society, 3, 54-64.

Packer, L., Monckton, S.K., Onuferko, T.M. & Ferrari, R.R. (2018) Validating taxonomic identifications in entomological research. Insect Conservation & Diversity, 11, 1-12.

Randolph, S. (2005) The Natural History of the Rose Bedeguar Gall and its Insect Community, The British Plant Gall Society.

Rennie, J. (1857) Insect Architecture. John Murray, London.

Rohwer, S. A. & Fagan, M. M. (1917) The type-species of the genera of the Cynipidea, or the gall wasps and parasitic cynipoids. Proceedings of the U.S. National Museum, 53, 357-380.

Shorthouse, J.D. (1973) The insect community associated with rose galls of Diplolepis polita (Cynipidae, Hymenoptera). Quaestiones Entomologicae, 9, 55-98.

Stille, B. (1984) The effect of hosptlant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae (Hymenoptera, Cynipidae). Oecologia, 63, 364-369.

Stille, B. & Dävring, L. (1980) Meiosis and reproductive strategy in the parthenogenetic gall wasp Diplolepis rosae (L.) (Hymenoptera, Cynipidae), Heriditas, 92, 353-362.

Urban, J. (2018). Diplolepis rosae (L.) Hymenoptera: Cynipidae): development, ecology and galls in the Brno region. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 66, 905-925.

Wakefield, P. (1816) An Introduction to the Natural History and Classification of Insects in a series of Familiar Letters with Illustrative Engravings. Darton, Harvey & Darton, London.

Walker, P., Leather, S.R. & Crawley, M.J. (2002) Differential rates of invasion in three related alien oak gall wasps (Cynipidae: Hymenoptera). Diversity & Distributions, 8, 335-349.

Weld, L. H. (1926) Field notes on gall-inhabiting cynipid wasps with descriptions of new species. Proceedings of the United States National Museum, 68, 1-131.

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-3032.1940.tb00573.x

https://www.britishplantgallsociety.org/bedeguar-keys.pdf

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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.

https://upload.wikimedia.org/wikipedia/commons/9/93/Diplolepis-rosae.jpg

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?

References

Becquaert, J. (1924) Galls that secrete 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.

 

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