Tag Archives: Prunus padus

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 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.

 

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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.

References

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.

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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

monumental-data

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

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

graph

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.

 

References

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

 

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Red, green or gold? Autumn colours and aphid host choice

“The falling leaves
Drift by my window
The falling leaves
Of red and gold”

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Red, green and gold, all on one tree

When Frank Sinatra sang Autumn Leaves he was almost certainly not thinking of aphids and I am pretty certain that the English lyricist, Johnny Mercer, who translated the words from the original French by Jacques Prévert wasn’t either 🙂

The colours we see in autumn are mainly due to two classes of pigment, the carotenoids (yellow-orange; think carrot) and the anthocyanins (red-purple).  Carotenoids are present in the leaves all year round but are masked by the green chlorophyll.  Chlorophyll breaks down in autumn, leaving the yellow carotenes visible.  The anthocyanins on the other hand are not formed until autumn (Sanger, 1971; Lee & Gould, 2002) and this mixture of pigments give us the colours that have inspired so many artists.

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Autumn Leaves Georgia O’Keeffe (1924) Tate Modern

To many, autumn starts with the appearance of the first turning leaves, to me it is the arrival of gynoparae* of the bird cherry-oat aphid (Rhopalosiphum padi) on my bird cherry (Prunus padus) trees.

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Bird cherry, Prunus padus, leaves on the turn.

Little did I know when I started my PhD in 1977 that almost thirty years later I would be part of a raging debate about the function of autumn colouration in woody plants. At the time I was interested in the colonisation patterns (or as I pretentiously termed it in my thesis ‘remigration’) of bird cherry aphids from their secondary grass and cereal host plants to their primary host bird cherry.  My study system was 30 bird cherry saplings divided between two cold frames in the Biology Compound at the University of East Anglia (Norwich).  Every day from the middle of August until leaf fall I checked every leaf of each tree, for gynoparae, males and oviparae, carefully noting the position of each leaf, its phenological stage and giving it a unique number. I repeated this in the autumns of 1978 and 1979.  The phenological stage was based on the leaf colour: green, mature; yellow, mature to senescent; red, senescent.  What I reported was that more gynoparae landed on green and yellow leaves than on red and that the gynoparae on green and yellow leaves survived for longer and produced more offspring (oviparae), than those on red leaves (Leather, 1981).   The gynoparae of the bird cherry aphid are quite special in that although as adults they do not feed (Leather, 1982), they do not land on bird cherry trees at random (Leather & Lehti, 1982), but choose trees that not only do their offspring (the oviparae) do better on, but that also favour those aphids hatching from eggs in the spring (Leather, 1986).  It should not have come as a surprise then, that when I analysed some of the data I had collected all those years ago, their preference for green and yellow leaves over red ones, is linked to how long those

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Figure 1. Length of time leaves remained on tree after first colonisation by gynoparae of Rhopalosiphum padi (F = 30.1 df 2/77, P <0.001)

leaves have left to live (Figure 1). The timing of events at this time of year, has, of necessity, got to be very precise. The egg-laying females (oviparae) are unable to develop on mature bird cherry leaves (Leather & Dixon, 1981), but it seems that the bird cherry aphid has this under control, making its decisions about the timing of the production of autumn forms (morphs) sometime in August (Ward et al., 1984).  All very sensible as far as I was concerned and that was as far as I took things.  Subsequent work by Furuta (1986) supported this in that he showed that maple aphids settled on and reproduced on green-yellow and yellow-orange leaves but avoided red leaves which had shorter life spans.

Jump forward fifteen years or so, and in a paper, that at the time, had somehow passed me by, the late great Bill Hamilton and Sam Brown (Hamilton & Brown, 2001) hypothesised that trees with an intense autumn display, similarly to those brightly coloured animals that signal their distastefulness with yellows, blacks and reds, were signalling their unsuitability as a host plant to aphids.  Like the costs imposed on insects that sequester plant toxins to protect themselves against predators, the production of anthocyanins responsible for the red autumn colouration is expensive, especially when you consider that the leaves have only a short time left to live (Hoch et al., 2001).  In autumn, trees and woody shrubs are normally mobilising resources in the leaves and moving them back into themselves ready to be used again the following spring (Dixon, 1963). Ecologists and evolutionary biologists were thus keen to explain the phenomenon in terms of trade-offs, for example, fruit flags that advertise the position of fruits for those trees that rely on seed dispersal by vertebrates (Stiles, 1982) or as ultra-violet screens to prevent tissue damage (Merzlyak & Gittelson, 1995).  Hamilton & Brown felt that these hypotheses were either, in the case of the fruit flag, only applicable to trees with fruit present and, in the latter, untenable. Instead they advocated the ‘signalling hypothesis’ which was based on the premise that trees that suffer from a lot of aphids (attacked by more than one species rather than by large numbers of a single species), invest in greater levels of defence and in autumn advertise this using bright warning colours.   The premise being, that although it is metabolically expensive for the plants to produce these colours, it is worth the investment if they result in a reduction in aphid attack.

This hypothesis was not without its detractors. Others suggested, that far from avoiding red colours, aphids were attracted to yellow or green as an indicator of host nutrition (Wilkinson et al., (2002).  Holopainen & Peltonen (2002) also suggested that birch aphids use the onset of autumn colours to pick out those trees where nutrient retranslocation was happening, and thus with higher levels of soluble nitrogen in the leaves.  This was of course, what I was trying to confirm back when I was doing my PhD.  Conversely, supporters of the signalling hypothesis, argued that trees (birch again) that could ‘afford’ to produce bright autumn colours were fitter, so more resistant in general and that they were warning potential herbivores of this by a bright autumn display (Hagen et al 2004).

Round about this time (2002), I was approached by a young Swiss researcher, Marco Archetti, who knew that I had a plot of sixty bird cherry trees that I had planted up when I arrived at Silwood in 1992, originally designed to follow-up some work that I had begun whilst at the Forestry Commission looking at the effects of early season defoliation on subsequent tree growth (Leather, 1993, 1995).  Marco convinced me that I had the ideal set-up to test the ‘signalling hypothesis’ and what was to be a very fruitful collaboration began.

We counted arriving gynoparae and their offspring (oviparae) throughout October (Marco making trips over from Oxford where he was then based**) noting leaf colour before and after each count.  As with my PhD work we found that the greener trees were preferentially colonised by the gynoparae and that more oviparae were produced on those trees and that given what I had found earlier that bird cherry aphid gynoparae chose trees that are good hosts in spring (Leather, 1986), Marco felt that we were able to support the honest signalling hypothesis (Archetti & Leather, 2005).  I was slightly less comfortable about this, as there are only two species of aphid that attack bird cherry and one of those is very rare and the original signalling hypothesis was based on the premise that it was trees that were attacked by a lot of aphid species that used the red colouration as a keep clear signal.  Anyway, it was published 🙂

That said, others agreed with us, for example, Schaefer & Rolshausen (2006) who called it the defence indication hypothesis, arguing that bright colours advertise high levels of plant defence and that the herbivores would do well to stay away from those plants displaying them. On the other hand, Sinkkonen (2006) suggested that reproductively active plants produce autumn colours early to deter insects from feeding on them and thus reduce their seed set.

Chittka & Döring (2007) on the other hand, suggested that there is no need to look further than yellow carotenoids acting as integral components of photosynthesis and protection against light damage and red anthocyanins preventing photo-inhibition (Hoch et al., 2001) as to why trees turn colourful in autumn.  In other words, nothing to do with the insects at all.  A couple of years later however, Thomas Döring and Marco got together with another former colleague of mine from Silwood Park, Jim Hardie, and changed their minds slightly.  This time, whilst conceding that red leaves are not attractive to aphids but noting that yellow leaves are even more attractive than green ones, suggested that the red colour could be being used to mask yellow (Döring et al., 2009).

Others have their own pet theories.  In recent years, veteran Australian entomologist Tom White has become interested in the concept of insect species that specifically feed on senescent plant tissue (White, 2002, 2015) and added to the debate by suggesting that aphids in general are senescence feeders and thus choose green and yellow as they have longest time to live and that the red leaves are also nitrogen depleted (White, 2009) which is supported by my PhD data (Figure 1).  This resulted in a spirited response by Lev-Yadun & Holopainen (2011) who claimed that he had misunderstood the scenario in thinking that leaves go sequentially from green to yellow to red, which they suggest is rare (I question this) and that actually in trees that go from green to red, the leaves still contain significant amounts of nitrogen, so a deterrent signal is still required.

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Maple, green to yellow in this case

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Spindle, Euonymus europaeus, green to red

What about those trees and other plants that have red or purple leaves in the spring or all year round and not just in autumn?

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Some trees have red foliage all year

Trees like some of the ornamental cherries or copper beech? I haven’t been able to find any papers that suggest that red or purple-leaved varieties of beech and cherries are less susceptible to aphid attack.  My own observations, probably imperfectly recalled, are that copper beech is regularly infested by the beech woolly aphid, Phyllaphis fagi , and just as heavily, if not more so than the normal green-leaved  beech trees.  That of course may just be a reflection that the white waxy wool covering the aphid stands out more against the red leaves.  Perhaps someone out here might like to check this out?  Some work that my friend and former colleague, Allan Watt, (sadly unpublished) did many years ago in Scotland looking at the effect of beech species and cultivar on infestation levels by the beech leaf mining weevil, Rhynchaenus fagi, did not indicate any differences between copper and green cultivars.  It does seem however, that in cabbages, leaf colour can tell the specialist cabbage aphid, Brevicoryne brassciae, if plants are well defended or not, the bluer the cabbage, the nastier it is (Green et al, 2015).

To summarise:

  1. Red leaves are produced by the trees in autumn to reduce ultraviolet damage and protect metabolic processes in the leaf.
  2. Red leaves are deliberately produced by the tree to warn aphids that their leaves are well defended – honest signalling.
  3. Red leaves are produced by the tree to ‘fool’ the herbivores that the leaves are likely to drop soon and warn them to keep away so as to safeguard their fruit – dishonest signalling.
  4. The tree is blissfully unaware of the aphids and the aphids are exploiting the intensity of the autumn colours produced by the trees to select which are the best trees to colonise in terms of nutrition and length of time left on the tree.

As I write, the debate still goes on and we seem no nearer to arriving at a definitive answer to the riddle of why trees produce bright leaves in autumn.  If nothing else however, the debate has generated a lot of interest and enabled people to sneak some amusing titles into the scientific literature.  Do make the effort to read the titles of some of the references below.

References

Archetti, M. (2009) Phylogenetic analysis reveals a scattered distribution of autumn colours. Annals of Botany, 103, 703-713.

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.

Chittka, L. & Döring, T.F. (2007) Are autumn foliage colors red signals to aphids? PLoS Biology , 5(8): e187. Doi:10.1371/journal.pbio.0050187.

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Döring, T.F., Archetti, M. & Hardie, J. (2009) Autumn leaves seen through herbivore eyes.  Proceedings of the Royal Society London B., 276, 121-127.

Furuta, K. (1986) Host preferences and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera: Aphididae). Zeitschrift fur Angewandte Entomologie, 102, 93-100.

Green, J.P., Foster, R., Wilkins, L., Osorio, D. & Hartley, S.E. (2015) Leaf colour as a signal of chemical defence to insect herbivores in wild cabbage (Brassica oleracea).  PLoS ONE, 10(9): e0136884.doi:10.1371/journal.pone.0136884.

Hagen, S.B. (2004) Autumn coloration as a signal of tree condition. Proceedings of the Royal Society London B, 271, S184-S185.

Hamilton, W.D. & Brown, S.P. (2001) Autumn tree colours as handicap signal. Proceedings of the Royal Society London B, 268, 1489-1493.

Hoch , W.A.,  Zeldin, E.L. & McCown, B.H. (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology, 21, 1-8.

Holopainen, J.K. & Peltonen, P. (2002) Bright colours of deciduous trees attract aphids: nutrient retranslocation hypothesis.  Oikos, 99, 184-188.

Leather, S.R. (1981) Reproduction and survival: a field study of the gynoparae of the bird cherry-oat aphid, Rhopalosiphum padi (L.). Annales Entomologici Fennici, 47, 131-135.

Leather, S.R. (1982) Do gynoparae and males need to feed? An attempt to allocate resources in the bird cherry-oat aphid Rhopalosiphum padiEntomologia experimentalis et applicata, 31, 386-390.

Leather, S.R. (1986) Host monitoring by aphid migrants: do gynoparae maximise offspring fitness? Oecologia, 68, 367-369.

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

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.

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on its primary host. Annals of Applied Biology, 99, 115-118.

Leather, S.R. & Lehti, J.P. (1982) Field studies on the factors affecting the population dynamics of the bird cherry-oat aphid, Rhopalosiphum padi (L.) in Finland. Annales Agriculturae Fenniae, 21, 20-31.

Lee, D.W. & Gould, K.S. (2002) Anthocyanins in leaves and other vegetative organs: An introduction. Advances in Botanical Research, 37, 1-16.

Lev-Yadun, S. & Holopainen, J.K. (2011) How red is the red autumn leaf herring and did it lose its red color? Plant Signalling & Behavior, 6, 1879-1880.

Merzlyak, W.N. & Gittelson, A. (1995) Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescing leaves (Acer platanoides L.). Journal of Plant Physiology, 145, 315-320.

Sanger, J.E. (1971) Quantitative investigations of leaf pigments from their Inception in buds through autumn coloration to decomposition in falling leaves.  Ecology, 52, 1075-1089.

Schaefer, H.M. & Rolshausen, G. (2006) Plants on red alert – do insects pay attentionBioEssays, 28, 65-71.

Sinkkonen, A. (2006) Do autumn leaf colours serve as reproductive insurance against sucking herbivores?  Oikos, 113, 557-562.

Stiles, E.W. (1982) Fruit flags: two hypotheses. American Naturalist, 120, 500-509.

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

White, T.C.R. (2003) Nutrient translocation hypothesis: a subsect of the flush-feeding/senescence-feeding hypothesis. Oikos, 103, 217.

White, T.C.R. (2009) Catching a red herring: autumn colours and aphids. Oikos, 118, 1610-1612.

White, T.C.R. (2015) Senescence-feesders: a new trophic subguild of insect herbivore. Journal of Applied Entomology, 139, 11-22.

Wilkinson, D.M., Sherratt, T.N., Phillip, D.M., Wratten, S.D., Dixon, A.F.G. & Young, A.J. (2002) The adaptive significance of autumn colours.  Oikos, 99, 402-407.

 

 *for a detailed account of the wonderful terminology associated with aphid life cycles read here

**coincidentally he is now a Lecturer at the University of East Anglia in the same Department where I did my PhD

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Filed under Aphidology, Aphids, Science writing

Mellow Yellow – Not all aphids live on green leaves

I have written before about aphids and how their quest for the ideal food plant may explain the evolution of host alternation; we find that most aphid species tend to be associated with rapidly growing meristems, or newly flushing leaves (Dixon, 2005). Some aphids are so keen on young plant tissue that they ‘engineer’ youth in their host plants, injecting salivary compounds and forming leaf–rolls, pseudo-galls and galls, all of which act as nutrient sinks and lengthen the time that the modified leaves stay green and nutrient-rich

leaf roll Rhopalosiphum

 Leaf-roll caused by Rhopalosiphum padi on bird cherry, Prunus padus.

Leaf roll Myzus cerasi

Pronounced leaf roll pseudo-gall caused by Myzus cerasi on Prunus avium.

Non host-alternating (autoecious) aphids, such as the sycamore aphid Drepanosiphum platanoidis, the maple aphid, Periphyllus testudinaceus, or the birch aphid, Euceraphis punctipennis, have no such escape route; they are confined to their tree host for the year, albeit, they can, if they ‘wish’, fly to another tree of the same species, but essentially they are held hostage by the their host plant. As the season progresses, leaf nutritional and physical properties change; going from young tender green leaves, with high nitrogen and water contents, to mature, tough leaves, low in nitrogen and water to yellow senescing leaves with again, higher nitrogen levels (Awmack & Leather, 2002) and finally of course, dead brown leaves of no nutritional value.

Seasonal changes

Sycamore and maple aphids, enter a state of suspended animation ‘summer aestivation’ (Essig, 1952; Dixon, 1963), whilst birch and poplar aphids, whose hosts plants often produce new growth during the year, ‘track’ these new leaves (Wratten, 1974; Gould et al., 2007). As far as these aphids are concerned young tissue is their best food source, with senescent tissue being second best and mature leaves being least favoured. During the summer they will, however, take advantage of mature leaves that are prematurely senescing, such as those attacked by leaf diseases such as tar spot. I have often found sycamore aphids feeding and reproducing on these infected leaves whilst those aphids on neighbouring mature leaves remain in aestivation.

Tar spot 2

Effects of tar spot on sycamore leaves

Host-alternating (heteroecious) aphids on the other hand are somewhat different. As their life cycle includes a programmed migration back to their primary tree host in autumn, those autumn morphs (oviparae) are adapted to senescent tissue (Leather & Dixon, 1982, Kundu & Dixon, 1993, 1994). Similarly, the spring morphs (fundatrices and fundatrigeniae) are adapted to young leaves and find it difficult or impossible, to make a living on senescent leaves.
Morphs and host age

There are yet other aphids, such as the green spruce aphid Elatobium abietinum, the pine aphid, Eulachnus agilis and the black pecan aphid, Melanocallis caryaefoliae, that are senescence specialists. In contrast to the flush specialists, these aphids engineer senescence, also using salivary compounds,  and are unable to survive on young foliage (Bliss, 1973; Fisher, 1987; Cottrell et al., 2009).

Elatobium in action

Elatobium abietinum ‘engineering’ senescence on spruce needles and avoiding young flushing tissue.

It is interesting to speculate that perhaps these tree-dwelling non host-alternating aphids are secondarily derived from the autumn part of the life-cycle of host-alternating aphids. After all, if non host-alternating aphids on herbaceous host plants are off-shoots of the summer part of the host-alternating life-cycle why not the other way round. There is just so much more to learn about aphids. Yet another reason why I love aphids so much 😉

References

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

Bliss, M., Yendol, W.G., & Kearby, W.H. (1973) Probing behaviour of Eulachnus agilis and injury to Scotch pine. Journal of Economic Entomology, 66, 651-655.

Cottrell, T.E., Wood, B.W. & Ni, X. (2009) Chlorotic feeding injury by the Black Pecan Aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environmental Entomology, 38, 411-416.

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Dixon, A.F.G. (2005) Insect Herbivore-Host Dynamics. Cambridge University Press, Cambridge.

Fisher, M. (1987) The effect of previously infested spruce needles on the growth of the green spruce aphid, Elatobium abietinum. Annals of Applied Biology, 111, 33-41.

Gould, G.G., Jones, C.G., Rifleman, P., Perez, A., & Coelman, J.S. (2007) Variation in Eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behaviour of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae). Environmental Entomology, 36, 1212-1225.

Kundu, R. & Dixon, A.F.G. (1993) Do host alternating aphids know which plant they are on? Ecological Entomology, 18, 61-66.

Kundu, R. & Dixon, A.F.G. (1994) Feeding on their primary host by return migrants of the host alternating aphid, Cavariella aegopodii. Ecological Entomology, 19, 83-86.

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.

Wratten, S.D. (1974) Aggregation in the birch aphid, Euceraphis punctipennis (Zett.) in relation to food quality. Journal of Animal Ecology, 43, 191-198.

 

Post script

A lot of what I describe comes from a talk I gave in 2009 at a workshop in Oxford on autumn colours (the output of which was Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., & Thomas, H. (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology & Evolution, 24, 166-173. I always meant to write the talk up as an Opinion piece but procrastination set in badly. I was somewhat annoyed with myself when earlier this year this excellent piece by the legendary ecologist and entomologist, Tom White, appeared; I have only myself to blame, six years is a very long bit of procrastination 😉

White, T.C.R. (2015) Senescence-feeders: a new trophic sub-guild of insect herbivores Journal of Applied Entomology, 139, 11-22.

 

Post post script

This post is dedicated to my eldest son, Sam, who died quietly in his sleep, at a tragically young age, December 23rd 2010.   It would have been his birthday on the 21st May.  Despite being a molecular biologist, (he worked at the Sanger Institute), he was as green as you can get, a great naturalist and conservationist, with an incredibly gentle soul. He strongly believed in conserving the World’s natural resources and amused colleagues by sticking up signs in the toilets at the Sanger, which read “If its yellow let it mellow, if its brown flush it down”.

Sampsa

 

He is sorely missed by us all. He also had more Nature papers than me 😉

Parkhill, J., Achtman, M., James, K.D. et al., (2000) Complete DNA sequence of a serogroup A strain of Neisseria meningitides. Nature, 404, 502-506

Parkhill, J., Dougan, G. , James, K.D. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature, 413, 848-852.

Parkhill, J., Wren, B.W., Thomson, N.R. et al., (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523-527.

Parkhill, J., Sebaihia, M., Preston, A. et al., (2003) Comparative analysis of the genome sequences of Bordetella pertussis,   Bordetella parapertussis and Bordetella bronchiseptica. Nature Genetics, 35, 32-40

Wood, V., Gwilliam, R. Rajandream, M.A. et al., (2002) The genome sequence of Schizosaccharomyces pombe . Nature, 415, 871-880

 

 

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Not all Aphids are Pests

Unfortunately when you mention the word aphid most people’s first thought is PEST!  It is true that they are perhaps the most important insect pests of crops

Larson             Punk aphid

in temperate regions of the world, and that in the UK they are serious pests of cereals, sugar beet, beans, vegetables and glasshouse crops.  It has been estimated that crop losses due to feeding damage and/or virus transmission exceed £100 million per annum http://www.scri.ac.uk/research/pp/pestanddisease/insectmiteecology/virusvectorinteractions .  On the other hand this is down to only about 250 species which out of a total of 5000 described species is not very many (about 5%).  Not only are most aphids playing useful roles in ecosystems acting as food sources to other insects, arthropods and dare I say it, vertebrates 😉 . They also play an important part in the decomposition cycle (Choudhury, 1985).  The thing that most people don’t realise is that some aphids are incredibly rare. Some are rare because of their close associations with rare plants, others rare because of a complex relationship with ants https://simonleather.wordpress.com/2013/12/05/not-all-aphids-live-on-leaves/ and some for no apparent reason at all.  For example, there are two aphid species that live on bird cherry (Prunus padus),  Rhopalosiphum padi, an extremely common aphid, host-alternating between bird cherry and grasses, and a major pest of cereals in temperate countries (Leather et al., 1989) and Myzus padellus, host-alternating between bird cherry and members of the Labiatae (Galeopsis spp. (Hemp nettle)) and Scrophulariaceae (Pedicularis spp. and Rhinanthus sp., members of the snapdragon family).  In all my many years of sampling bird cherry I have never seen Myzus padellus, yet their life-cycles and habits are strikingly similar, so why is the latter so rare?  No one knows.

Similarly, on birch we find, not very often because it is so rare, Monaphis antennata , which unlike most aphids, lives as a nymph (immature) on the upper side of birch leaves, possibly

Monaphis

to escape natural enemies as the much more common species of birch aphids, Euceraphis punctipennis and Betulaphis quadrituberculata like the majority of leaf-feeding aphids, both live on the underside of leaves, which is where aphid predators normally forage (Hopkins & Dixon 1997). I have seen this aphid once, shown to me by the late Nigel Barlow http://newzealandecology.org/nzje/free_issues/NZJEcol30_1_1.pdf  when he visited me at Silwood Park in the late 1990s.  Despite repeated visits to the same trees that we found Monaphis on, I have never seen it again.  So far no one has been able to explain why it is so rare (Hopkins et al., 1998).  Interestingly enough, apart from keys and identification manuals, it has rarely been written about; Web of Knowledge reveals only four research papers on it.

There are many more rare aphids hiding out there, a number of which have only ever been seen by the entomologist who first described them and no doubt even more who have not yet been found, as is the cases with many more insect species  – not enough insect taxonomists, not enough funding.

Choudhury, D. (1985) Aphid honeydew – a re-appraisal of Owen and Wiegert’s hypothesis. Oikos, 45, 287-289. http://www.jstor.org/discover/10.2307/3565718?uid=3738032&uid=2&uid=4&sid=21103382740253

Hille Ris Lambers, D. & Rogerson, J.P. (1946) A new British aphid from Prunus padus L.  Myzus padellus sp n. (Hemiptera, Aphididae). Proceedings of the Royal Entomological Society of London, 15, 101-105 http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3113.1946.tb00833.x/abstract

Hopkins, G.W. & Dixon, A.F.G. (1997) Enemy-free space and the feeding niche of an aphid. Ecological Entomology, 22, 271-274. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2311.1997.00075.x/full

Hopkins, G.W. & Dixon, A.F.G. (2000)  Feeding site location in birch aphids (Sternorrhyncha: Aphididae): the simplicity and reliability of cues.  European Journal of Entomology, 97, 279-280 http://www.eje.cz/pdfs/eje/2000/02/19.pdf

Hopkins, G.W., Thacker, J.I., & Dixon, A.F.G. (1998) Limit to the abundance of rare species: an experimental test with a tree aphid. Ecological Entomology, 23, 386-390. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2311.1998.00163.x/full

Leather, S.R., Walters, K.F.A., & Dixon, A.F.G. (1989) Factors determing the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), in Europe: a study and review. Bulletin of Entomological Research, 79, 345-360. http://journals.cambridge.org/download.php?file=%2FBER%2FBER79_03%2FS0007485300018344a.pdf&code=8d6d2144666846ebb5d589f01343f27c

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Silk- not just a spider thing

Mention silk and most people will, I guess, immediately think of spiders and cobwebs.

Pressed a bit further, some may mention silkworms, and some might even know the word sericulture and that the common silkworm feeds on mulberry bushes.   What they may not know, is that the silk worm is the larvae of the moth Bombyx mori and that there are actually four species of lepidopteran larvae commonly used in silk production.  These are pictured below in the lovely illustration from Meyers Konversations-Lexikon; next to the picture are some B. mori larvae.

Silkworm larvae Silkworms

Meyers Konversations-Lexikon, 4th Auflage, Band 14, Seite 826a (4th ed., Vol. 14, p.826a)

Four of the most important domesticated silk moths. Top to bottom: Bombyx mori, Hyalophora cecropia, Antheraea pernyi, Samia cynthia. From Meyers Konversations-Lexikon (1885-1892

Silk production is of course not just a feature of spiders and lepidoptera.  It is a widespread feature of insect life, being used for pupal cases, as a mode of transport (ballooning) as shown by larvae of the gypsy moth and other species of Lepidoptera,

ballooning gypsy moth            ballooning gypsy moth drawing

protective cases as in larval caddis flies or also, by some caddis fly larvae, as fishing equipment.

 caddisfly_larva  Caddis fly net

But in my opinion, the most dramatic use of silk is that seen in a genus of micro-moths, belonging to the Yponomeutidae, the small ermine moths, Yponomeuta.  They and their relatives, are silk-producers extraordinaire.  Collectively, they are known as small ermine moths; so called because of their adult colouration which resembles the ermine worn by nobility and small, because of the existence of several larger moths with ermine in their names.

Yponomeuta_evonymellus

http://commons.wikimedia.org/wiki/File:Yponomeuta_evonymella-02_(xndr).jpg#file

The larvae are less attractive and are the web/silk producers.

Yponomeuta_evonymella_caterpillars

http://commons.wikimedia.org/wiki/File:Yponomeuta.evonymella.caterpillars.jpg

My particular favourite is the bird cherry ermine moth, and not just because the bird cherry is my favourite tree.  (My eldest son’s middle name is bird cherry, albeit in Finnish). The adult moths lay their eggs in August, in clusters of up to 100 or so on young twigs of the bird cherry Prunus padus, cover them with an egg shield and then die (Leather, 1986).  The eggs hatch shortly afterwards and the larvae spend the winter under the egg shield until the following spring.  When the buds begin to burst in spring, the larvae emerge from beneath the shield and begin to feed gregariously on the newly emerging leaves, spinning a web that protects them from natural enemies  and may also help in thermoregulation and as a trail indicator (Kalkowski, 1958)  http://edepot.wur.nl/201846 .  It is possible to have great fun by selecting a lead larvae to act as a trail blazer and watch the rest of the colony follow them to a destination you have chosen.

Every three to four years or so, populations of the moths get so high that they exhaust their food supplies, defoliating entire trees and covering  them with a tough coating of silky white webbing (Leather, 1986; Leather & Mackenzie, 1994).  In fact, in Finland, I once saw three neighbouring trees totally enveloped in a silken tent caused by the bird cherry ermine moth, Yponomeuta evonymellus, that you could enter and shelter inside from the rain.  Once they really get going as spring progresses, the landscape, particularly if in an area where bird cherry is common, begins to take on a somewhat wintry look, which for May is a little odd.  Those of who you, who have travelled north of Perth in Scotland, on the A9, will be familiar with this phenomenon.  It frequently makes the Scottish newspapers and generates headlines such as “winter wonderland” or “ghostly landscape”. As they run out of trees, the larvae begin to migrate in a desperate search for trees with leaves still on them, and by now, have become less fussy about what they eat.  It is at this wandering stage of their life that the true extent

Yponomeuta webbing  bird cherry emrine moth webbing

of their singlemindedness (I have seen a trail of thousands of larvae marching along a railway line; they didn’t survive the passing of the 0850 from Helsinki) and their ability to produce silk becomes startlingly apparent.

Ermine moths on car    Ermine_moth_larva_on_a_Swedish_army_bike

http://commons.wikimedia.org/wiki/File:Ermine_moth_larva_on_a_Swedish_army_bike.jpg

Truly, silk is not just a spider thing.

Kalkowski, W. (1958). Investigations on territorial orientation during ontogenic development in Hyponomeuta. Folia Biol Krakow 6: 79-102.

Leather, S. R. & Mackenzie, G. A. (1994). Factors affecting the population development of the bird cherry ermine moth, Yponomeuta evonymella L. The Entomologist 113: 86-105.

Leather, S. R. (1986). Insects on bird cherry I The bird cherry ermine moth, Yponomeuta evonymellus(L.). Entomologist’s Gazette 37: 209-213.

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