Tag Archives: aphids

Prunella – mistress of plasticity

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

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

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

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

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

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

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

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

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

 

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

References

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

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

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

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

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

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

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

 

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Pick and mix 9 – a few links to click

Links to things I thought might grab your fancy

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

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

Communicating entomology through video

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

How bees see may help us develop better cameras

How bumblebee flight may help us develop better drones

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

Interesting article on insect symbolism in 19th Century British art

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

This account of sexism in academia shocked and horrified m

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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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Not all aphids are farmed by ants

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

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

antsaphids-1

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

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

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

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

antsaphids-2

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

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

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

antsaphids4

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

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

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

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

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

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

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

antsaphids5

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

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

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

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

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

Aren’t insects wonderful?

 

References

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

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

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

Dixon, A.F.G. (1958a) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London, 110, 319-334.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

*in my opinion at any rate 🙂

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

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

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

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

 

Post script

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

antsaphids-holdrich

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

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Insects in flight – whatever happened to the splatometer?

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

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

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

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

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

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

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

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

 

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

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The “Splatometer” as designed by the RSPB

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

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

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

splat-4

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

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

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

Post script

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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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”

red-green-or-gold-1

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.

red-green-or-gold-2

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

red-green-or-gold-4

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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An aphid is… a flea, a louse, and even a marine mammal!

Earlier this year I wrote about the debate that rages about the correct way to talk about thrips during which I got distracted and ended up writing about their names in different languages. It turns out that I am not alone in being curious about international insect naming. I have just finished reading Matthew Gandy’s excellent book Moth, where he waxes lyrical about the different names used to describe butterflies and moths around the world.  This, of course, made me wonder what aphid would turn up, so armed with dictionaries and Google Translate, I traveled the world to see what I could discover.

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The bronze-brown dandelion aphid, Uroleucon taraxaci – Photo by Jasper Hubert

There are a lot of languages so I am only going to highlight a few versions of aphid that I found interesting or surprising.  According to The Oxford English Dictionary, Linneaus coined the word Aphides, which may (or not) have been inspired by the Ancient Greek  ἀφειδής‎ (apheidḗs) meaning unsparing, perhaps in relation to their rapid reproduction and feeding habits.  The modern spelling of aphid seems to have come into being after the Second World War, although you could still find aphides being used in the late 1940s (e.g. Broadbent et al., 1948; Kassanis, 1949), and it can still be found in more recent scientific literature where the journal is hosted in a non-English speaking country.

Many aphid names are very obviously based on the modern Latin word coined by Linneaus, although in some countries more than one name can be used, as in the UK where aphid is the technical term but blackfly and green-fly are also commonly used.

 

Aphide derived names

Albanian              afideja

English                  aphid

French                  aphide

Hindu                    एफिड ephid

Portuguese         afídio

Spanish                áfido

 

More common are those names that relate to the vague resemblance that aphids have to lice and to their plant feeding habit. The term plant lice to describe aphids was commonly used in the scientific literature up and into the early 1930s (e.g. Mordvilko, 1928; Marcovitch, 1935).

 

Names linked to the putative resemblance to lice and their plant feeding habit

Bosnian                lisna uš                 uš is louse, lisna derived from leaf

Bulgarian             listna vŭshka     vŭshka louse, listna plant leaf

Danish                  bladlaus               blad is leaf, laus louse

Dutch                    bladluis                blad is leaf, luis is louse

Estonian               lehetäi                  leht is leaf, tai is louse

German                Blattlaus               blatt is leaf, laus is louse

Greek                   pseíra ton fytón louse on plant

Hungarian           levéltetű               leve is leaf, tetű is louse

Icelandic              lús or blaðlús     lús is louse, blað is plant

Latvian                  laputs                   lapa is, uts is louse

Norwegian          bladlus                 blad is plant, lus is louse

Swedish               bladlus                 as for Norwegian

 

If you draw siphunculi on to a louse and add a cauda to the rear end you can just about see the resemblance.

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Louse with added siphunculi and cauda

 

Names based on the premise that aphids resemble fleas

French  puceron                  puce is flea

Spanish pulgón                   pulga is flea

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Flea with cauda and siphunclus, but still only a poor imitation of the real thing.  Even with added aphid features I don’t see the resemblance 🙂

 

In Turkish, aphid is yaprak biti which roughly translates to leaf biter.  There are then a few languages where there appears to be no connection with their appearance or feeding habit.

 

Other names for aphid

Basque                 zorri

Chinese                蚜

Filipino                 dapulak

Finnish                  kirva

Lithuanian           Mszyca

Tamil                     அசுவினி Acuviṉi

Welsh                   llyslau

Xhosa                    zomthi

 

In Lithuanian, where aphid is Mszyca, which looks like it might be derived from Myzus, an important aphid genus, aphid also translates to amaras which means blight.  In the case of a heavy aphid infestation, this is probably an apt description.  I was also amused to find that whilst the Welsh have a name for aphid, Scottish Gaelic does not.

My all-time favourite, and one for which I can find no explanation at all, is dolphin.  According to Curtis (1845), aphids on cereals in some counties of England were known as wheat dolphins.  I was also able to trace the use of this name back to the previous century (Marsham, 1798), but again with no explanation why this name should have arisen.

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The wheat dolphin 🙂

References

Broadbent, L., Doncaster, J.P., Hull, R. & Watson, M.A. (1948) Equipment used for trapping and identifying alate aphides.  Proceedings of the Royal Entomological Society of London (A), 23, 57-58.

Curtis, J. (1845) Observations on the natural history and economy of various insects etc., affecting the corn-crops, including the parasitic enemies of the wheat midge, the thrips, wheat louse, wheat bug and also the little worm called Vibrio. Journal of the Royal Agricultural Society, 6, 493-518.

Gandy, M. (2016) Moth, Reaktion Books, London

Kassanis, B. (1949) The transmission of sugar-beet yellows virus by mechanical inoculation. Annals of Applied Biology, 36, 270-272.

Marcovitch, S. (1935) Experimental evidence on the value of strip farming as a method for the natural control of injurious insects with special reference to plant lice. Journal of Economic Entomology, 28, 62-70.

Marsham, T. (1798) XIX. Further observations on the wheat insect, in a letter to the Rev. Samuel Goodenough, L.L.D. F.R.S. Tr.L.S.  Transactions of the Linnaean Society of London, 4, 224-229.

Mordvilko, A. (1928) LXX.—The evolution of cycles and the origin of Heteroecy (migrations) in plant-lice , Annals and Magazine of Natural History: Series 10, 2, 570-582.

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It isn’t easy being an applied ecologist – working on crops limits publication venues

“This is Simon Leather, he’s an ecologist, albeit an applied one” Thus was I introduced to a group of visiting ecologists by my then head of department at the Silwood Park campus of Imperial College. As you can imagine I was somewhat taken aback at this public display of the bias that ‘pure’ scientists have against those that they regard as ‘applied’.  I was (and still am), used to this attitude, as even as an undergraduate doing Agricultural Zoology when we shared modules with the ‘pure’ zoologists, we were regarded as a slightly lower life form J  Working in Finland as a post-doc in the early 1980s it was also obvious that there was a certain degree of friction between the pure and applied entomologists, so it was not a phenomenon confined entirely to the UK.  To this day, convincing ecology undergraduates that integrated pest management is a suitable career for them is almost impossible.

I was an ecologically minded entomologist from early childhood, pinning and collecting did not interest me anywhere near as much as insect behaviour and ecology, but I knew that I wanted to do something “useful” when I grew up. Having seen my father in action as a plant pathologist and crop protection officer, it seemed to me that combining entomology with agriculture would be an ideal way to achieve this ambition.  A degree in Agricultural Zoology at Leeds and a PhD in cereal aphid ecology at the University of East Anglia (Norwich) was the ideal foundation for my chosen career as an applied ecologist/entomologist.

I started my professional life as agricultural entomologist working both in the laboratory and in the field (cereal fields to be exact), which were easily accessible, generally flat, weed free and easy to manipulate and sample.  In the UK even the largest fields tend to be visible from end to end and side to side when you stand in the middle or edge (even more so now than when I started as wheat varieties are now so much shorter, less than half the height they were in 1977).

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Having fun as a PhD student – aphid ‘sampling’ in Norfolk 1978

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I haven’t grown since I did my PhD so wheat must have shrunk 🙂

See the post script to see what wheat used to look like.

Laboratory experiments, even when working on mature plants were totally do-able in walk-in growth rooms, and at a push you could even fit whole earing wheat plants into a growth cabinet.

I then spent ten years working as a forest entomologist, where field sites were the exact opposite, and extreme measures were sometimes required to reach my study animals, including going on an official Forestry Commission tree climbing course.

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Pole pruners – (of only limited use) and tree climbing (great fun but laborious)

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Scaffold towers for really high work, but expensive (and scary on sloping hillsides).

And as for lab work, not a chance of using mature plants or even plants more than two to three years old.  Excised branches and/or foliage (rightly or wrongly) were the norm*.

Doing field work was, despite the sometimes very physically challenging aspects, a lot of fun, and in my case, some very scenic locations.  My two main field sites were The Spey Valley and

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Sutherland and Caithness, both of which provided magnificent views and of course, a plethora of whisky distilleries

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where I discovered what is now my favourite single malt 🙂

The real fun came when it was time to submit papers.  Journal choice was (and is) very important.  As Stephen Heard points out, journals have a ‘culture’ and it is very important to pick a journal that has the right editorial board and ethos. The laboratory work never seemed to be a huge problem, referees (perhaps wrongly) very rarely criticised the use of young plants or excised foliage. I was able to publish the output from what was a very applied project, in a range of journals from the very specialised to the more ecological. This selection for example, from 1985-1987 (Leather, 1985, 1986; Leather & Burnand, 1987; Leather et al., 1985), appeared in Ecological Entomology, Oecologia, Functional Ecology and Bulletin of Entomological Research respectively.

Papers reporting field-based work were a little bit harder to place in journals outside the mainstream forestry ones, particularly when it came to experimental work.  One of the problems was that ecological referees unused to working in forests tended not to have a grasp of what was involved in setting up and servicing an experiment in a forest plantation or stand.  A farmer has no great objection to an entomologist removing 100 wheat tillers a week from his 2 ha field (at 90 stems per metre2, even a 16 week field season would only remove a tiny fraction of his crop).  A forest manager on the other hand with a stocking density of 3000 stems per hectare would look askance at a proposal to remove even 100 trees a month from a hectare plot, especially if this was repeated for seven years.  Sample size was thus a problem, even when using partial sampling of trees, e.g. by removing say only one branch.  When it came to field scale replication, to compare for example, three treatments and a control on two different soil types, where each treatment plot is a hectare, things get a bit difficult. The most that we could service, even with help (since we did not have huge financial resources), was three replicates of each treatment.  In agricultural terms this seems incredibly low, where 10m2 plots or even smaller, are very often used (e.g. Staley et al., 2009; Garratt et al., 2011).

We thus ended up with our experimental papers in the really specialised forestry journals (e.g.  Leather, 1993; Hicks et al., 2007).  On the other hand, those papers based on observational, long-term data were easier to place in more general ecological journals (e.g. Watt et al., 1989), although that was not always enough to guarantee success (e.g. Walsh et al., 1993; Watt et al., 1991).  Another bias that I came across (perhaps unconscious) was that referees appeared, and still do, think that work from production forests is not as valid as that coming from ‘natural’ forests, especially if they are tropical. We came across this when submitting a paper about the effects of prescribed burning on carabid populations in two sites in Portugal (Nunes et al., 2006).  We originally sent this to a well-known ecological journal who rejected it on the grounds of low replication, although we had also replicated it temporarily as well as geographically.  I was not impressed to see a paper published in this journal shortly after they had rejected our manuscript in which the authors had reported changes in insect communities after a one-off fire event in a tropical forest, without even the benefits of pre-fire baseline data.  We had in the meantime, given up on general ecology journals and submitted our paper to a local forestry journal.  Such is life.

I originally started this essay with the idea of bemoaning the fact that publishing studies based in production forests in more general journals was more difficult than publishing agriculturally based papers, but got diverted into writing about the way applied ecologists feel discriminated against by journals and pure ecologists.  I may or may not have convinced you about that.  To return to my original idea of it being more difficult for forestry–based ecologists to break out of the forestry journal ghetto than it is for agro-ecologists to reach a broader audience, I present the following data based on my own publication record, which very convincingly demonstrates that my original feeling is based on fact, albeit based on an n of one 🙂

applied-fig-7

Numbers of agricultural and forestry based papers published by me in different journal categories.

I might also add that being an entomologist also limits where you can publish, so being an applied entomologist is something of a double whammy, and when it comes to getting research council funding, don’t get me started!

References

 Garratt, M.P.D., Wright, D.J., & Leather, S.R. (2010) The effects of organic and conventional fertilizers on cereal aphids and their natural enemies. Agricultural and Forest Entomology, 12, 307-318.

Hicks, B.J., Aegerter, J.N., Leather, S.R., & Watt, A.D. (2007) Differential rates of parasitism of the pine beauty moth (Panolis flammea) depends on host tree species. Scottish Forestry, 61, 5-10.

Leather, S.R. (1985) Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecological Entomology, 10, 213-217.

Leather, S.R. (1986) The effect of neonatal starvation on the growth, development and survival of larvae of the pine beauty moth Panolis flammea. Oecologia, 71, 90-93.

Leather, S.R. (1993) Influence of site factor modification on the population development of the pine beauty moth (Panolis flammea) in a Scottish lodgepole pine (Pinus contorta) plantation. Forest Ecology & Management, 59, 207-223.

Leather, S.R. & Burnand, A.C. (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D&S): the hidden costs of reproduction. Functional Ecology, 1, 331-338.

Leather, S.R., Watt , A.D., & Barbour, D.A. (1985) The effect of host plant and delayed mating on the fecundity and lifespanof the pine beauty moth,  Panolis flammea (Denis & Schiffermuller) (Lepidoptera: Noctuidae): their influence on population dynamics and relevance to pest management. Bulletin of entomological Research, 75, 641-651.

Nunes, L.F., Silva, I., Pité, M., Rego, F.C., Leather, S.R., & Serrano, A. (2006) Carabid (Coleoptera) community change following prescribed burning and the potential use of carabids as indicator species to evaluate the effects of fire management in Mediterranean regions. Silva Lusitania, 14, 85-100.

Staley, J.T., Stewart-Jones, A., Pope, T.W., Wright, D.J., Leather, S.R., Hadley, P., Rossiter, J.T., Van Emden, H.F., & Poppy, G.M. (2010) Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments. Proceedings of the Royal Society of London B, 277, 779-786.

Walsh, P.J., Day, K.R., Leather, S.R., & Smith, A.J. (1993) The influence of soil type and pine species on the carabid community of a plantation forest with a history of pine beauty moth infestation. Forestry, 66, 135-146.

Watt, A.D., Leather, S.R., & Stoakley, J.T. (1989) Site susceptibility, population development and dispersal of the pine beauty moth in a lodgepole pine forest in northern Scotland. Journal of Applied Ecology, 26, 147-157.

Watt, A.D., Leather, S.R., & Evans, H.F. (1991) Outbreaks of the pine beauty moth on pine in Scotland: the influence of host plant species and site factors. Forest Ecology and Management, 39, 211-221.

 

Post script

The height of mature wheat and other cereals has decreased hugely over the last two hundred years.  Cereals were originally a multi-purpose crop, not just providing grain for humans, but bedding straw for stock and humans, winter fodder for animals, straw for thatching and if really desperate, you could make winter fuel out of discarded straw**.

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John Linnell  – Wheat 1860  You wouldn’t have been able to see Poldark’s (Aidan Turner) manly chest whilst he was scything in this field!

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Pieter Breugel the Elder – Die Kornernter – The Harvesters  (1565) – Head-high wheat crops and not just because the average height was lower in those days.

 

*As I was writing this article I came across this paper (Friberg & Wiklund, 2016) which suggests that using excised plants may be justifiable.  Friberg, M. & Wiklund, C. (2016)  Butterflies and plants: preference/performance studies in relation to plant size and the use of intact plants vs. cuttings.  Entomologia experimentalis et applicata, 160, 201-208

**My source for this is Laura Ingalls Wilder – Little House on the Prairie, to be exact 🙂

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