Tag Archives: Rhopalosiphum padi

On rarity, apparency and the indisputable fact that most aphids are not pests

I am willing to bet that when most entomologists are out for a walk spend most of their time looking at the ground or the vegetation between the ground and head height. Lepidopterists and odonatologists may be the exceptions that prove the rule, but most of us spend a lot of time looking for things lurking in dung, hiding under stones or bark, scurrying around in the undergrowth or making holes in leaves 🙂

Tell-tale signs for an entomologist that something is or has been enjoying a meal

I’m an entomologist, I’m trained to look out for signs of insect infestations; curled leaves as in the above picture tell me that almost certainly an aphid and her offspring have been at work, sticky leaves alert me to the fact that there are aphids above me in the canopy of a tree. Leaves with holes tell me that a beetle or caterpillar has been at work. Leaves spun together with a silk web tell me a similar story. Plants with their stems and leaves stripped right back inform me that sawfly, lepidoptera and beetle larvae have been at work. A fancy spiral of brown or white on a leaf tells me that a leafminer has been, or is at work. In some cases the insect may not be there when I see the damage, the curled leaves caused by an aphid or psyllid infestation remain there until leaf fall, the chances of finding a caterpillar feeding on the very obviously shot-holed leaves of a plant are slim.  Like all sensible herbivores, the culprit will be in hiding closer to the stem, only sporadically popping out to feed.  On the other hand it may have fallen victim to a visually acute predator (bird) that was attracted to the leaf by the tell-tale feeding signs, or been eaten by a predatory insect or  have been parasitized by an ichneumonid wasp.  Plants are a lot less passive than people think. By producing the equivalent of an immune response they cause the insects to move to different feeding sites to make more holes effectively advertising their presence to potential predators.  Simultaneously, the plant sends out chemical signals telling insect predators and parasites that there is a meal or host available.  An herbivore’s lot is not an easy one.

The Covid-19 crisis means that I have been working from home in a hamlet on the Staffordshire/Shropshire border.  To keep myself reasonably sane and moderately physically healthy I have been treating myself to a lunchtime walk along the bridleways, footpaths and public roads within a 5 km radius of my house. As a result I have become much more familiar with the area. One of the things that has been very obvious, apparent even, is that some plants dominate the roadside verges, cow parsley Anthricus sylvestris being one that really stands

Cow parsley – very common and abundant, occurring in huge swathes around Forton and Sutton and in this case and in many other sites along my walks, backed by the equally apparent hawthorn (Crataegusus monogyna) hedge.

out from the crowd at this time of the year. Not only is it very apparent, but it provides a great source of nectar for the spring butterflies such as the Orange Tip and the assorted bumblebees, solitary bees and hoverflies, that despite the anthropogenic pressures put upon them, still manage to make an appearance.  Nettles, as I particularly noticed when having to social distance myself from the sweaty joggers and cyclists taking advantage of the virtually deserted country lanes, also play a prominent role in the roadside plant community. Also very common, but showing a much patchier distribution and occurring in clumps, including in my garden, is the ribwort plantain, Plantago lanceolata, which is yet another so called weed*, that is perfect for pollinators.

Ribwort plantain – common but patchy and clumped – this clump in my garden where it is safe from forks and herbicides.

Although both the cow parsley and plantain were buzzing with pollinators, they were, and still are at time of writing, singularly devoid of herbivores, including my favourite aphids. Conversely, the odd scattered bird cherries (Prunus  padus) and the solitary self-seeded wild cherry (Prunus avium) in my garden are proudly sporting the characteristic leaf rolls caused by the bird cherry aphid, Rhopaloisphum padi and the cherry black fly, Myzus cerasi respectively.

Note that both these trees were not growing near any of their relatives and were surrounded and overtopped by other plant species, so as far as humans are concerned not very apparent.

This got me to wondering why it was, that, the to me, and presumably other humans, the very obvious cow parsley and plantains, were not covered in plant feeding insects, while the less apparent cherries were heavily infested by their respective aphids.  After all, according to Richard Root, large swathes of monocultures are likely to be easily found and colonised by pests. Plant apparency was first defined by the British born, American based ecologist Paul Feeny in the mid-1970s.

“The susceptibility of an individual plant to discovery by its enemies may be influenced not only by its size, growth form and persistence, but also by the relative abundance of its species within the overall community. To denote the interaction of abundance, persistence and other plant characteristics which influence likelihood of discovery, I now prefer to describe “bound to be found” plants by the more convenient term “apparent”, meaning “visible, plainly seen, conspicuous, palpable, obvious” (Shorter Oxford English Dictionary, 3rd, edition; Webster’s Concise English Dictionary). Plants which are “hard to find” by their enemies will be referred to as “unapparent”, the antonym of apparent (O.E.D. and Webster, loco cit.). The vulnerability of an individual plant to discovery by its enemies may then be referred to as its “apparency”, meaning “the quality of being apparent; visibility” (O.E.D. and Webster, loco cit.). Since animals, fungi and pathogens may use means other than vision to locate their host-plants, I shall consider apparency to mean “susceptibility to discovery” by whatever means enemies may employ” Feeny (1976).

So, even though cow parsley is highly visible and apparent to us humans, and their pollinators, because it is an annual and thus ephemeral within the landscape, it is not necessarily apparent to the herbivores that want to feed on it. Conversely, trees, such as bird cherry, although not necessarily apparent to us, are apparent to insect herbivores because they are large and long-lived. How does this affect the way in which plants avoid being found and eaten by insect herbivores?

Peter Price, another British born American based ecologist very neatly summarised Paul’s hypothesis as follows

Long-lived trees which are bound to be found by herbivores, invest heavily in costly chemical defence with broad-spectrum efficacy.   These quantitative defences are expensive but the cost is tolerable for a long-lived plant.  Short-lived plants are less easily detected by herbivores, and their best defence is being hard to find in patchy and ephemeral sites.  Low cost defences are effective against generalist herbviores should plants be found.  Instead of tannins and other digestibility reducers found as defences in long-lived plants, short-lived plants have evolved with mustard oils (glucosinolates) in crucifers, for example, alkaloids in the potato family, furanocoumarins in the carrot family (Price, 2003).

All I can say is that the quantitative defences of the trees don’t seem to be doing as good a job as the less expensive ones of the cow parsley, plantains and nettles.  As an aside, it turns out that although both cow parsley and plantain have a lot of medicinal uses, their chemistry does include some insecticides (Adler et al., 1995; Milovanovic et al., 1996). Cheap and cheerful seems to be the answer for an herbivore-free life in this case 🙂 Earlier I referred to cow parsley and plantains as being common.  What does that mean? According to Wikipedia (where else would I go?),

 “Common species and uncommon species are designations used in ecology to describe the population status of a species. Commonness is closely related to abundance. Abundance refers to the frequency with which a species is found in controlled samples; in contrast, species are defined as common or uncommon based on their overall presence in the environment. A species may be locally abundant without being common.

However, “common” and “uncommon” are also sometimes used to describe levels of abundance, with a common species being less abundant than an abundant species, while an uncommon species is more abundant than a rare species.”

In the UK we have a conservation designation, Sites of Special Scientific Interest, the criteria for selection which can be found here. To save you the trouble of reading the whole document, the way in which rarity and scarcity are defined is as follows.

Nationally Rare (15 or fewer UK hectad (10 km squares) records)

Nationally Scarce – Notable A (31-100 UK hectad records),

Nationally Scarce – Notable B (16-30 hectad records.

Local – (101-300 UK hectad records)

Okay, so what has all this to do with aphids and their pest status? As you all probably know by now I love aphids; as far as I am concerned, where insects are concerned, they are the bee’s knees**.

Unfortunately, aphids get a terrible press, most of it, in my opinion, undeserved.

Just a couple of examples of aphids getting a biblically bad press.

A few years ago, I wrote a short piece about the fact that only a minority of the so far 5600 or so aphids described, are pests, and many are very rare. The cover of this issue of New Scientist from 1977, which appeared a few months after I joined the group, very nicely sums up the question that we really ought to be asking. Here I have to confess that the article from our lab (McLean et al., 1977), made the case for aphids being pests, and it was the late Denis Owen who defended aphids (Owen, 1977).

Tony Dixon’s cereal aphid research group (of which I was proud to be a member) got more than just a mention in this issue.

Two plants that I have a particular interest in are sycamore and bird cherry, mainly because of their aphids, but in the case of the bird cherry, I love its flowers.  Now, although both have very similar distributions and occurrences to cow parsley and ribwort plantain, ubiquitous, they are much easier

Distribution of cow parsley, ribwort plantain, and sycamore and bird cherry in the British Isles (Atlas of the British Flora)

to find aphids on than both cow parsley and plantain.  On my daily walks during which I pass countless cow parsley and plantain plants, I have, so far, only found one cow parsley with aphids on and not a single plantain has shown any signs of aphid infestation . I have also, only found one nettle plant with Microlophium carnosum on it.  Cow parsley has a number of aphid species that use it as a secondary host migrating there from willows or hawthorns. Plantains also serve as host plants to aphids, some such as Dysaphis plantaginea host alternate, others such as Aphis plantaginis, do not. The latter species, if present, is almost always ant attended (Novgorodova & Gavrilyuk, 2012), which, if you know what you are looking for, makes it easy to spot.  I know what to look for and so far, have not found any! Nettles are also very common in the roadside verges, and they too have aphids that love them, Microlophium carnosum and Aphis urticata, the former a favourite prey of ants, the latter, farmed by the ants.  So far this year I have only found one small colony of M. carnosum, and believe me, I have been looking.

So what about the trees? Sycamores are a common sight on my walks, occurring both as hedges and as solitary trees or sometime in small groups. Almost all the large trees have sycamore aphids, Drepanosiphum platanoidis feeding on their leaves, and many have dense colonies of the maple aphid, Periphyllus testudinaceus, some with ants in attendance. Bird cherry is not as common on my walks and where I have found it, they have been small trees or shrubs usually on their own, and surrounded by other woody plants. Without exception, all have been conspicuously infested by the bird-cherry oat aphid.  To summarise, we have common plants that support aphids that are not regarded as rare, but find startlingly different levels of abundance of them here in Staffordshire, and in my experience, elsewhere.  At the same time that I have been actively searching for aphids, six species of butterfly that the Woodland Trust lists as common, have been hard to miss.  In order of sightings these are the Orange Tip, the Peacock, the Small Tortoiseshell, the Speckled Wood, the Holly Blue and the Brimstone, two of which, the Peacock and the Small Tortoiseshell, being nettle feeders as larvae. Despite the abundance of nettles in the hedgerows, So far I have only seen one small colony of Small Tortoiseshell larvae on the of nettles. I am, at this juncture, unable to resist mentioning that adults of the Holly Blue feed on aphid honeydew J Going back to my original point, the fact that I have seen more butterflies than aphids doesn’t necessarily mean that the aphids are less abundant, just less apparent.

There are at least 614 species of aphid in the UK (Bell et al., 2015). I am not sure how many I have seen, I stopped keeping a personal tick list many years ago, but I would guess that I have seen about half of them.  I like aphids, I look for aphids, but there are many ‘common’ species that I have never seen. I have, however, seen some of the rare ones. Four that stand out in my memory are Monaphis antnenata, Stomapahis graffii, Myzocallis myricae and Maculolachnus submacula. The first feeds on the upper surface of birch leaves (Hopkins & Dixon, 1997) and was shown to me by the late Nigel Barlow, when he was on a sabbatical at Silwood Park. Stomaphis graffii which feeds under the bark of sycamores and maples and is ant attended, was shown to me by an MSc student, Andrew Johnson, also at Silwood Park.  Myzocallis myricae, the bog myrtle aphid, only found on bog myrtle (Myrica gale) (Hopkins et al., 2002), I saw in the Highlands of Scotland, when Tony Dixon asked me to stop the car so he could go and look at a clump of bog myrtle he had spotted as we drove along between field sites. The giant rose aphid, Maculolachnus submacula, I saw in my garden in Norwich (84 Earlham Road) when I was a PhD student at the University of East Anglia.  I only found it because I wondered why there was an ant nest reaching halfway up one of my roses.  When I looked, I found that they were farming the aphids that were feeding on the lower stems.

It is important to remember that most aphids are host-specific, some feeding only on a single plant species, others being confined to a single genus with only a minority having a wide host range*** and considered pests (Dixon, 1998). Given this, it is obvious that aphids with rare host plants are also going to be rare (Hopkins et al., 2002).  Many aphids are also very fussy about their niche, either feeding on a very particular part of a plant or having a very close association with a particular species of ant.  Looking at the aphids that the two Bobs (Influential Points it seems that aphids that are rare  are also ant-attended.  Given, that many ant-attended aphids aren’t rare it would seem an interesting area to pursue. Perhaps it is the degree of ant-attendance, i.e. facultative versus obligate that is the key factor?

If you look at the list of species of insects that are regarded as endangered and worthy of conservation in the UK, the overwhelming impression is that unless they are big and pretty they don’t get a look in.  Needless to say, despite their beauty and fascinating life styles, no aphids are included in the list L

We really should be conserving aphids, not squashing them. Many provide important nutrition for ants and other pollinators, honeydew.  They are an important source of food for insects and birds (Cowie & Hinsley, 1988).  Aphids also help plants grow by feeding mycorrhizae with their honeydew (Owen, 1980; Milcu et al., 2015). Finally, as aphids are so host specific using the presence of uncommon species in suction traps could help identify sites with rare plants.

Aphids, rare, useful and much maligned, time to rethink their role.

 

References

Adler, L.S., Schmitt, J. & Bowers, M.D. (1995) Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia, 101, 75-85.

Bell, J.R., Alderson, L., Izera, D., Kruger, T., Parker, S., Pickup, J., Shortall, C.R., Taylor, M.S., Verier, 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.

Cowie, R.J. & Hinsley, S.A. (1988) Feeding ecology of great tits (Parus major) and blue tits (Parus caeruleus), breeding in suburban gardens. Journal of Animal Ecology, 57, 611-626.

Dixon, A.F.G. (1998) Aphid Ecology. Chapman & Hall, London.

Feeny, P. (1976) Plant apparency and chemical defence. Recent Advances in Phytochemistry, 10, 1-40.

Hopkins, G.W. & Dixon, A.F.G. (1997) Enemy-free space and the feeding niche of an aphid. Ecological Entomology, 22, 271-274.

Hopkins, G.W., Thacker, J.I.T., Dixon, A.F.G., Waring, P. & Telfer, M.G. (2002) Identifying rarity in aphids: the importance of host plant range. Biological Conservation, 105, 293-307.

McLean, I., Carter, N. & Watt, A. (1977) Pests out of Control. New Scientist, 76, 74-75.

Milcu, A., Bonkowski, H., Collins, C.M. & Crawley, M.J. (2015) Aphid honeydew-induced changes in soil biota can cascade up to tree crown architecture. Pedobiologia, 58, 119-127.

Milovanovic, M., Stefanovic, M., Djermanovic, V., & Milovanovic, J. (1996). Some chemical constituents of Anthriscus sylvestris. Journal of Herbs, Spices & Medicinal Plants, 4, 17–22. Eugenol – insecticide

Novgorodova, T.A. & Gavrilyuk, A.V. (2012). The degree of protection different ants (Hymenoptera: Formicidae) provide aphids (Hemiptera: Aphididae) against aphidophages European Journal of Entomology, 109, 187-196.

Owen, D.F. (1977) Are aphids really plant pests? New Scientist, 76, 76-77.

Owen, D.F. (1980) How plants may benefit from the animals that eat them. Oikos, 35, 230-235.

Price, P.W. (2003) Macroecological Theory on Macroecological Patterns, Cambridge University Press, Cambridge.

Thacker, J.I., Hopkins, G.W. & Dixon, A.F.G. (2006) Aphids and scale insects on threatened trees: co-extinction is a minor threat. Oryx, 40, 233-236.

Uusitalo, M. (2004) European Bird Cherry (Pruns padus L). A Biodiverse Wild Plant for Horticulture. MTT Agrifood Research Finland, Jokioinen.

** https://en.wiktionary.org/wiki/the_bee%27s_knees    

***Hugh Loxdale however, would argue that all insects are specialists and that so called polyphagous species are, in reality, cryptic specialist species (Loxdale, H.D., Lushai, G. & Harvey, J.A. (2011) The evolutionary improbablity of ‘generalism’ in nature, with special reference to insects. Biological Journal of the Linnean Society, 103, 1-18.)

 

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Filed under Aphidology, Aphids

An unintended consequence – Maris Huntsman: A great choice for entomological careers but not so good for farmers

I could have used Sod’s Law or Murphy’s Law as the lead in for this article, but as you will see (if you keep on reading), this story isn’t all doom and gloom 😊. During the 1960s, cereal growers in the UK and on mainland Europe, were subjected to onslaughts on two fronts, yellow rust* ((Puccinia striiformis) (Doling & Doodson, 1968) and cereal aphids (Fletcher & Bardner, 1969; Kolbe, 1969).  Although cereal aphids had been a sporadic problem in Europe for several decades previously (Kolbe, 1969,1973; Rautapää, 1976) and even earlier than that (e.g. Marsham, 1798), 1968 was an exceptional year for them (Fletcher & Bardner, 1969; Kolbe, 1969).  Presaging  Richard Root’s seminal work on crop apparency and pest occurrence, the Dutch agronomist Willem Feekes predicted that changes in agricultural practice, in particular cereal production, would lead to increased pest and disease problems (Feekes, 1967). This was further emphasised by Wilhelm Kolbe of Bayer, who suggested that the big increase in cereal production in Europe between 1950 and 1970 and the switch from oats to wheat was the cause of the cereal aphid problem (Kolbe, 1973).   Similarly, in the UK, where oats were 51% of the cereal crop in 1930, they had fallen to 11% by 1965 (Marks & Britton, 1989).

Cereal production UK

The shift in cereal crops may indeed have been a contributory factor, but I think, certainly in the UK, that we can add another factor to the equation. Over at Maris Lane**, where the Plant Breeding Institute was based at Trumpington, Cambridge, a new variety of wheat, Maris Huntsman, with good resistance to both powdery mildew and yellow rust (Ruckenbauer, 1975) had been developed and introduced as a recommended variety to farmers in 1972 (Hughes & Bodden, 1978).  By 1977 it accounted for almost 40% of the wheat sold in the UK (Hughes & Bodden, 1978), although a mere two years later, it had fallen to just over 20% (Johnson, 1992).  Based at Trumpington, entomologist Henry Lowe, had, since the late1960s been investigating the resistance of crop plants to aphids, first beans (e.g. Lowe, 1968) was at the time, investigating the resistance of varieties of wheat to aphids (Lowe, 1978, 1980). He found, as one might expect that not all cereal species and varieties were equally susceptible to aphids, and if given a free choice, the grain aphid Sitobion avenae, showed a preference for Maris Huntsman.

So what does this have to do with launching the careers of a couple of dozen entomologists? Well, back in the late 1960s Tony Dixon, then based in Glasgow, got interested in the bird cherry-oat aphid, Rhopalosiphum padi  (Dixon, 1971; Dixon & Glen, 1971), a minor pest of cereals in the UK, mainly because of its great ability to transmit Barley Yellow Dwarf Virus (Watson & Mulligan, 1960. In those countries, such as Finland and Sweden, where spring sown cereals are the norm, it is a pest in its own right, able to cause yield reduction without the help of a virus (Leather et al., 1989). Tony moved to the University of East Anglia as Professor of Ecology in 1975 and started his new career there by appointing six new PhD students. Three of these were looking at aspects of cereal aphid ecology, Allan Watt researching the biology of S. avenae and Metoplophium dirhodum, Ian McLean looking at the predators and Nick Carter modelling their populations in order to develop a forecasting system.  Research groups at Imperial College and at the University of Southampton also began to work on the problem.  Fortuitously although cereal aphid numbers had fallen since the  

Numbers of Sitobion avenae caught in the Brooms Barn suction trap (data from Watson & Carter, 1983)

populations picked up in 1974 and then rose to outbreak levels again in 1976, just as the new PhD students started their field work. I joined the group in 1977 to work on R. padi, followed in subsequent years by Keith Walters (now a colleague at Harper Adams University), John Chroston, Sarah Gardner, Nigel Thornback, Ali Fraser, Shirley Watson, Trevor Acreman, Dave Dent, and after I left for pastures new, Alvin Helden (now Head of School at Anglia Ruskin University). Similar numbers of students were appointed at Southampton, including Nick Sotherton, now Director of Research at the Game and Wildlife Conservation Trust.  There were also groups started at Imperial College and the University of Reading. There was a certain element of rivalry between the groups, Steve Wratten for example, was an ex-student of Tony’s and there was a certain degree of animosity between Roy Taylor (of Taylor’s Power Law fame) at Rothamsted and Tony Dixon, we had mini-conferences to exchange findings and generally got on well.  Allan Watt for example went to work for Steve Wratten as a post-doc before moving up to Scotland to work on the pine beauty moth alongside me.  It was a great time to be working on aphids and I think we all benefitted from the experience and I for one, am very grateful to the plant breeders for developing a  variety of wheat, that although resistant to rust and powdery mildew, is very attractive to the grain aphid 🙂

Having fun in a Norfolk cereal field; me, Allan Watt and Ian McLean (Nick Carter had the good sense to stand behind the camera).

You may be wondering why I penned this reminiscence. Well, last year, my colleague Tom Pope and I were discussing cereal aphids at coffee time (as you do), and I mentioned how Maris Huntsman had launched my career.  It just so happened that Tom had access to old, ancient and modern varieties of cereals to hand and a final year project student keen on aphids so it doesn’t take a genius to guess what happened next 🙂

Host preferences of Sitobion avenae (Dan Hawes & Tom Pope). Can you guess which is Maris Huntsman?

So, Maris Huntsman, a great choice for attracting aphids and producing entomologists 🙂 and of course a great big vote of thanks to the PBI

 

References

Dean, G.J.W. & Luuring, B.B. (1970) Distribution of aphids on cereal crops. Annals of Applied Biology, 66, 485-496.

Dixon, A.F.G. (1971) The life cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi (L) and its bearing on the theory of host alternation in aphids. Annals of Applied Biology, 68, 135-147.

Dixon, A.F.G. & Glen, D.M. (1971) Morph determination in the bird cherry-oat aphid, Rhopalosiphum padi (L). Annals of Applied Biology, 68, 11-21.

Doling, D.A. & Doodson, J.K. (1968) The effect of yellow rust on the yield of spring and winter wheat. Transactions of the British Mycological Society, 51, 427-434.

Feekes, W. (1967) Phytopathological consequences of changing agricultural methods. II Cereals. Netherlands Journal of Plant Pathology, 73 Supplement 1, 97-115.

Fletcher, K.E. & Bardner, R. (1969) Cereal aphids on wheat. Report of the Rothamsted Experimental Station 1968, 200-201.

Hughes, W. G., & Bodden, J. J. (1978). An assessment of the production and performance of F1 hybrid wheats based on Triticum timopheevi cytoplasm. Theoretical and Applied Genetics, 53, 219–228.

Janson, H.W. (1959) Aphids on cereals and grasses in 1957. Plant Pathology, 8, 29.

Johnson R. (1992) Past, present and future opportunities in breeding for disease resistance, with examples from wheat. [In] Johnson R., Jellis G.J. (eds) Breeding for Disease Resistance. Developments in Plant Pathology, vol 1. Springer, Dordrecht

Kolbe, W. (1969) Studies on the occurrence of different aphid species as the cause of cereal yield and quality. Pflanzenschutz Nachrichten Bayer, 22, 171-204.

Kolbe, W. (1973) Studies on the occurrence of cereal aphids and the effect of feedingdamage on yields in relation. Pflanzenschutz Nachrichten Bayer, 26, 396-410.

Latteur, G. (1971) Evolution des populations aphidiennes sur froments d’hiver.  Mededelingen van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent, 36, 928-939.

Leather, S.R., Walters, K.F.A., & Dixon, A.F.G. (1989) Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae), in Europe: a study and review. Bulletin of Entomological Research, 79, 345-360.

Leather, S.R., Carter, N., Walters, K.F.A., Chroston, J.R., Thornback, N., Gardner, S.M., & Watson, S.J. (1984) Epidemiology of cereal aphids on winter wheat in Norfolk, 1979-1981. Journal of Applied Ecology, 21, 103-114.

Lowe, HJ.J.B. (1967) Interspecific differences in the biology of aphids (Homoptera: Aphididae) on leaves of Vicia faba I. Feeding behaviour. Entomologia experimentalis et applicata, 10, 347-357.

Lowe, H.J.B. (1974) Effects of Metopolophium dirhodum on Spring wheat in the glasshouse.  Plant Pathology, 23, 136-140.

Lowe, H.J.B. (1978) Detection of resistance to aphids in cereals.  Annals of Applied Biology, 88, 401-406.

Lowe, H.J.B. (1980) Resistance to aphids in immature wheat and barley. Annals of Applied Biology, 95, 129-135.

Macer, R.C.F. (1972) The resistance of cereals to yellow rust and its exploitation by plant breeding.  Proceedings of the Royal Society London B., 181, 281-301.

Marks, H.F. & Britton, D.K. (1989)  A Hundred  Years of British Food and Farming: A Statistical Survey. Taylor & Francis.

Marsham, T. (1798) 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 London, 4, 224-229.

Rautapää, J. (1976) Population dynamics of cereal aphids and method of predicting population trends. Annales Agriculturae Fenniae, 15, 272-293.

Rogerson, J.P. (1947) The oat-bird cherry aphis Rhopalosiphum padi (L.) and comparison with R. crataegellum Theo. Bulletin of Entomological Research, 38, 157-176.

Ruckenbauer, P.  (19 75) Photosynthetic and translocation pattern in contrasting winter wheat varieties. Annals of Applied Biology, 79, 351-359.

Watosn, M.A. & Mulligan, T. (1960) The manner of transmission of some Barley Yellow‐Dwarf Viruses by different aphid species. Annals of Applied Biology, 48, 711-720.

Watson, S.J. & Carter, N. (1983) Weather and modelling cereal aphid populations in Norfolk (UK). EPPO Bulletin, 13, 223-227.

Zayed, Y. & Loft, P. (2019) Agriculture: Historical Statistics. House of Commons Briefing paper 3339

 

*Yellow rust is still a  still a major problem for cereal growers worldwide

**an address that is immortalised in the names of several cultivars of crops developed by the PBI

 

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Satiable curiosity – side projects are they worthwhile?

I’ve been meaning to write this one for quite a while.  It was stimulated by two posts, one from the incredibly prolific Steve Heard, the other by the not quite so prolific, but equally interesting,  Manu Saunders.  First off, what is a side project?  To me, a side project is one that is not directly funded by a research council or other funding agency or, in some cases, one that you do in your spare time, or to the horror of some line-managers, is not strictly in your job description 🙂 The tyranny of modern research funding dictates that projects must have specific research questions and be accompanied by hypotheses and very specific predictions; most proposals I referee, even contain graphs with predicted results and almost all have ‘preliminary data’ to support their applications.   This is not necessarily a bad thing but to directly quote Manu Saunders from her blog post

“Whittaker’s (1952) study of ‘summer foliage insect communities in the Great Smoky Mountains’ is considered one of the pioneer studies of modern community ecology methods. The very short Introduction starts with the sentence “The study was designed to sample foliage insects in a series of natural communities and to obtain results of ecological significance from the samples.” No “specific research questions” and the hypotheses and predictions don’t appear until the Discussion” Sounds like bliss.

The central ethos of my research career which began in 1977, can be summed up by this quotation uttered by the character ‘Doc’ in John Steinbeck’s novel Sweet Thursday “I want take everything I’ve seen and thought and learned and reduce them and relate them and refine them until I have something of meaning, something of use” (Steinbeck, 1954).* The other thing that has driven me for as long as I can remember, and why I ended up where I am,  is something I share with Rudyard Kipling’s Elephant Child, and that is a “satiable curiosity”:-) Something that has always frustrated me, is that, in the UK at least, most funded research tends to be of a very short duration, usually three years, often less than that**, and if you are very lucky, maybe five years.  If you work on real life field populations, even if you work on aphids, these short term projects are not really very useful; laboratory work is of course a different matter.

I got my first ‘permanent’ job in 1982 working for UK Forestry Commission Research based at their Northern Research Station (NRS) just outside Edinburgh.  My remit initially was to work on the pine beauty moth, Panolis flammea and finally, on the large pine weevil, Hylobius abietis.  As a committed aphidophile, I was determined, job description or not, to carry on working with aphids. I decided that the easiest and most useful thing to do was to set up a long-term field study and follow aphid populations throughout the year.  My PhD was on the bird cherry-oat aphid, Rhopalosiphum padi, a host alternating aphid, the primary host of which is the bird cherry, Prunus padus, with which  Scotland is very well supplied, and fortuitously, just down the road from NRS was Roslin Glen Nature Reserve with a nice healthy population of bird  cherry trees.  I chose ten suitable trees and started what was to become a ten-year once a week, lunch time counting and recording marathon.  I also decided to repeat a study that my PhD supervisor, Tony Dixon had done, record the populations of the sycamore aphid, Drepanosiphum platanoidis.  In the grounds of NRS were five adjacent sycamore tree, Acer pseudoplatanus, and these became my early morning study subjects, also once a week. I had no articulated hypotheses, my only aim was to count and record numbers and life stages and anything else I might see. Anathema to research councils but exactly what Darwin did 🙂

Although it was a ‘permanent’ job, after ten years I moved to Imperial College at Silwood Park and immediately set up a new, improved version of my sycamore study, this time a once weekly early morning*** walk of 52 trees in three transects and with much more data collection involved, not just the aphids, their natural enemies and anything else I found and on top of all that, the trees themselves came in for scrutiny, phenology, growth, flowering and fruiting, all went into my data sheets.  I also set up a bird cherry plot, this time with some hypotheses articulated 🙂

As a result of my weekly walk along my sycamore transects, a few years later I set up yet another side project, this time an experimental cum observational study looking at tree seedling survival and colonisation underneath different tree canopies. At about the same time, initially designed as a pedagogical exercise, I started my study of the biodiversity of Bracknell roundabouts.

One might argue that most undergraduate and MSc research projects could also come under the heading of side projects, but I think that unless they were part of a long term study they aren’t quite the same thing, even though some of them were published.  So, the burning question, apart from the benefits of regular exercise, was the investment of my time and that of my student helpers and co-researchers worth it scientifically?

Side project 1.  Sycamore aphids at the Northern Research Station, 1982-1992

I collected a lot of aphid data, most of which remains, along with the data from Side project 2, in these two notebooks, waiting to be entered into a spreadsheet.  I also collected some limited natural enemy data, presence of aphid mummies and numbers killed by entomopathogenic fungi.  Tree phenological data is limited to bud burst and leaf fall and as I only sampled five trees I’m not sure that this will ever amount to much, apart from perhaps appearing in my blog or as part of a book.  Nothing has as yet made it into print, so a nil return on investment.

Raw data – anyone wanting to help input into a spreadsheet, let me know 🙂 Also includes the data for Side project 2

 

Side project 2.  Rhopalosiphum padi on Prunus padus at Roslin Glen Nature Reserve 1982-1992

I was a lot more ambitious with this project, collecting lots of aphid and natural enemy data and also a lot more tree phenology data, plus noting the presence and counting the numbers of other herbivores.  I have got some of this, peak populations and egg counts in a spreadsheet and some of it has made it to the outside world (Leather, 1986, 1993: Ward et al., 1998).  According to Google Scholar, Ward et al., is my 6th most cited output with, at the time of writing, 127 citations, Leather (1993) is also doing quite well with 56 citations, while Leather (1986) is much further down the list with a mere 38 citations.  I have still not given up hope of publishing some of the other aphid data.  I mentioned that I also recorded the other herbivores I found, one was a new record for bird cherry (Leather, 1989), the other, the result of a nice student project on the bird cherry ermine moth (Leather & MacKenzie, 1994).  I would, I think, be justified in counting this side project as being worthwhile, despite the fact that I started it with no clear hypotheses and the only aim to count what was there.

 

Side project 3.  Everything you wanted to know about sycamores but were afraid to ask 1992-2012

As side projects go this was pretty massive.  Once a week for twenty years, me and on some occasions, an undergraduate research intern, walked along three transects of 52 sycamore trees, recording everything that we could see and count and record, aphids, other herbivores, natural enemies and tree data, including leaf size, phenology, height, fruiting success and sex expression.  My aim was pretty similar to that of Whittaker’s i.e.   “…to sample foliage insects in a series of natural communities and to obtain results of ecological significance from the samples”  truly a mega-project.  I once calculated that there are counts from over 2 000 000 leaves which scales up to something like 10 000 000 pieces of data, if you conservatively estimate five data observations per leaf. Quite a lot of the data are now computerized thanks to a series of student helpers and Vicki Senior, currently finishing her PhD at Sheffield University, but certainly not all of it. In terms of output, only two papers so far (Wade & Leather, 2002; Leather et al., 2005), but papers on the winter moth, sycamore and maple aphids and orange ladybird are soon to be submitted.  On balance, I think that this was also worthwhile and gave me plenty of early morning thinking time in pleasant surroundings and a chance to enjoy Nature.

The sycamore project – most of the raw data, some of which still needs to be computerised 🙂

 

Side project 5. Sixty bird cherry trees 1993-2012

This project has already featured in my blog in my Data I am never going to publish series and also in a post about autumn colours and aphid overwintering site selection.  Suffice to say that so far, thanks to my collaborator Marco Archetti, two excellent papers have appeared (Archetti & Leather, 2005; Archetti et al., 2009), the latter of which is my third most cited paper with 101 cites to date and the former is placed at a very respectable 21st place.  I don’t really see any more papers coming out from this project, but I might get round to writing something about the study as a whole in a natural history journal. On balance, even though only two papers have appeared from this project, I count this as having been a very worthwhile investment of my time.

All now in a spreadsheet and possibly still worthwhile delving into the data

 

Side project 5.  Urban ecology – Bracknell roundabouts 2002-2012

This started as a pedagogical exercise, which will be the subject of a blog post in the not too distant future. The majority of the field work was done by undergraduate and MSc students and in the latter years spawned a PhD student, so a side project that became a funded project 🙂 To date, we have published seven papers from the project (Helden & Leather, 2004, 2005; Leather & Helden, 2005ab; Helden et al., 2012; Jones & Leather, 2012; Goodwin et al., 2017) and there are probably two more to come.  Definitely a success and a very worthwhile investment of my time.  The story of the project is my most requested outreach talk so also gives me the opportunity to spread the importance of urban ecology to a wider audience.

The famous roundabouts – probably the most talked and read about roundabouts in the world 🙂 Sadly Roundabout 1 i n o longer with us; it was converted into a four-way traffic light junction last year 😦

 

Side project 6.  Testing the Janzen-Connell Hypothesis – Silwood Park, 2005-2012

I mentioned this project fairly recently so will just link you to it here.  So far only one paper has come out of this project (Pigot & Leather, 2008) and I don’t really see me getting round to doing much more than producing another Data I am never going to publish article, although it does get a passing mention in the book that I am writing with former colleagues Tilly Collins and Patricia Reader.  It also gave undergraduate and MSc project students something to do.  Overall, this just about counts as a worthwhile use of my time.

Most of this is safely in a spreadsheet but the data in the notebooks still needs inputting

According to my data base I have published 282 papers since 1980 which given that I have supervised 52 PhD students, had 5 post-docs, and, at a rough estimate, supervised 150 MSc student projects and probably 200 undergraduate student projects doesn’t seem to be very productive 😦 Of the 282 papers, 125 are from my own projects, which leaves 139 papers for the post-docs and PhD students and 17 from the side projects.  Three of the papers published from the side projects were by PhD students, so if I remove them from the side projects that gives an average of 2.3 papers per side project and 2.4 papers per post-doc and PhD student.   So, in my opinion, yes, side projects are definitely worth the investment.

 

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.

Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., & Thomas, H. (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology & Evolution, 24, 166-173.

Goodwin, C., Keep, B., & Leather, S.R. (2017) Habitat selection and tree species richness of roundabouts: effects on site selection and the prevalence of arboreal caterpillars. Urban Ecosystems, 19, 889-895.

Helden, A.J. & Leather, S.R. (2004) Biodiversity on urban roundabouts – Hemiptera, management and the species-area relationship. Basic and Applied Ecology, 5, 367-377.

Helden, A.J. & Leather, S.R. (2005) The Hemiptera of Bracknell as an example of biodiversity within an urban environment. British Journal of Entomology & Natural History, 18, 233-252.

Helden, A.J., Stamp, G.C., & Leather, S.R. (2012) Urban biodiversity: comparison of insect assemblages on native and non-native trees.  Urban Ecosystems, 15, 611-624.

Jones, E.L. & Leather, S.R. (2012) Invertebrates in urban areas: a review. European Journal of Entomology, 109, 463-478.

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

Leather, S.R. (1989) Phytodecta pallida (L.) (Col., Chrysomelidae) – a new insect record for bird cherry (Prunus padus). Entomologist’s Monthly Magazine, 125, 17-18.

Leather, S.R. (1993) Overwintering in six arable aphid pests: a review with particular relevance to pest management. Journal of Applied Entomology, 116, 217-233.

Leather, S.R. & Helden, A.J. (2005) Magic roundabouts?  Teaching conservation in schools and universities. Journal of Biological Education, 39, 102-107.

Leather, S.R. & Helden, A.J. (2005) Roundabouts: our neglected nature reserves? Biologist, 52, 102-106.

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

Leather, S.R., Wade, F.A., & Godfray, H.C.J. (2005) Plant quality, progeny sequence, and the sex ratio of the sycamore aphid, Drepanoisphum platanoidis. Entomologia experimentalis et applicata, 115, 311-321.

Pigot, A.L. & Leather, S.R. (2008) Invertebrate predators drive distance-dependent patterns of seedling mortality in a temperate tree Acer pseudoplatanus. Oikos, 117, 521-530.

Steinbeck, J. (1954) Sweet Thursday, Viking Press, New York, USA.

Wade, F.A. & Leather, S.R. (2002) Overwintering of the sycamore aphid, Drepanosiphum platanoidis. Entomologia experimentalis et applicata, 104, 241-253.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

Whittaker, R.H. (1952) A Study of summer foliage insect communities in the Great Smoky Mountains. Ecological Monographs, 22, 1-44.

 

*

I was so impressed by this piece of philosophy that it is quoted in the front of my PhD thesis 🙂

**

My second post-doc was only for two years.

***

You may wonder why I keep emphasising early morning in relation to surveying sycamore aphids.  Sycamore aphids are very easy to disturb so it is best to try and count them in the early morning before they have a chance to warm up and become flight active.

 

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Aphids galore, les pucerons à gogo – UK-France Joint Meeting on Aphids – April 3rd to 5th 2019

The giant aphid – a fitting start to an aphid conference, albeit taxonomically suspect 😊

I have just returned from a very enjoyable two-day meeting at Rothamsted Research Station in Harpenden.  This was a follow-up to the very enjoyable meeting we had in Paris in 2015 which made me ask somewhat facetiously, if pea aphids ruled the world 😊 As with the Paris meeting, this recent meeting was jointly organised by Jean-Christophe Simon and Richard Harrington with some input by me.  There were ninety delegates, and not just from France and the UK; we had a keynote speaker from Japan, Tsutomu Tsuchida, and also speakers from Belgium, the Czech Republic, Germany, Ireland and Switzerland.

Tsumato Tsuchida, me, Richard Harrington, Julie Jaquiéry, Jean-Christophe Simon and Richard Blackman.

Our other three keynote speakers included two of the doyens of the aphid world, Roger Blackman and Helmut van Emden   and Julie Jaquiéry from the University of Rennes.  As with the Paris meeting, many of the talks were about the pea aphid and symbionts.  Other aphids did, however, get mentioned, including my favourite aphid, Rhopaloisphum padi, which featured in an excellent talk by PhD student Amma Simon from Rothamsted, who is supervised by one of my former students, Gia Aradottir.  There was an excellent poster session, a tribute to the late great, Ole Heie from Mariusz Kanturski, a fabulous film by Urs Wyss, which included shocking scenes of lime aphids being torn apart by vicious predators, and of course the conference dinner.

It would take too long to describe all the talks, so I will let the pictures tell the story of a very enjoyable meeting.  Hopefully we will all meet again in France in 2023.

Great talks and a packed lecture theatre

Food and chat

Very animated poster sessions

Three senior aphidologists in action,  Helmut Van Emden, Hugh Loxdale and Roger Blackman

Richard Harrington presenting Roger Blackman and ‘Van’ van Emden with the Award of the Golden Aphid – the lighting in the conference dining area was very peculiar 😊

Strange lighting at the conference dinner

From the Urs Wyss film– lime aphid moulting

The giant aphid having a quick snack

And in case you wondered, there were embryos inside the giant aphid 🙂

Many thanks to the Royal Entomological Society and BAPOA/INRA for funding.

And here are most of the delegates on the final day

Aphid SIG 2019

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Not all aphid galls are the same

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

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Filed under Aphidology, Aphids

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

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

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

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

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

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

The grand plan!

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

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

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

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

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

The Sixty Tree site April 2006.

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

 

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

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

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

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

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

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

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

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

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

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

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

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

Number of Prunus padus trees with severe deer damage

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

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

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

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

References

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

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

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

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

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

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

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

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

 

 

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

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

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Ideas I had and never followed up

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

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

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

monumental-data

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

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

the-forgotten-nine

The Forgotten Nine

 

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

graph

In those days we used graph paper 🙂

 the data, do let me know.

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

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

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

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

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

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

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

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

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

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

 

References

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

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

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

Leather, S.R. (1988) Size, reproductive potential and fecundity in insects: Things aren’t as simple as they seem. Oikos, 51, 386-389.

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

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

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

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

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

 

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

**Now Vice-Chancellor of the University of Wollongong

 

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

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

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.

red-green-or-gold-3

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.

red-green-or-gold-5

Maple, green to yellow in this case

red-green-or-gold-6

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?

red-green-or-gold-7

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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Not all aphids get lost

Although aphids are very good at kicking, we know that aphids would not be very good at football as they are very short-sighted (Doring et al., 2008) but does that mean that they are not very good at finding their host plants? There is a common misperception, and not just confined to non-entomologists, that aphids are no more than aerial plankton. In 1924 Charles Elton

Lost 1

whilst on an expedition to Nordaustlandet* (the second largest of the Spitsbergen group and almost entirely covered by ice) reported finding large numbers of aphids, many still alive, later identified as Dilachnus piceae (now known as Cinara piceae) (Elton, 1925).

Lost 2

Cinara piceae the Greater Black Spruce Aphid –big and beautiful.

 

He suggested that the aphids came from the Kola Peninsula, a distance of about 800 miles (almost 1300 km) due to the strong south and south-east winds blowing at the time. He estimated that they would have made the journey within twelve to twenty-four hours. This was regarded as being an example of totally passive migration and used as one of many examples of aerial plankton** (Gislen, 1948). This is, however, probably not giving aphids credit for what they are capable of doing when it comes to flight. Berry & Taylor (1968), who sampled aphids at 610 m above the grounds using aeroplanes, implied that the aphids, although using jet streams, were flying rather than floating (page 718 and page 720) and that they would descend to the ground in the evening and not fly during the night.

Lost 3

Aphids don’t usually fly during the night. (From Berry & Taylor (1968)).

Dixon (1971) interprets this somewhat differently and suggests that the “movement of the air in which it is flying determines the direction of its flight and the distance it will travel” but then goes on to say “after flying for an hour or two aphids settle indiscriminately on plants”. So yes the speed of the air in which the aphid is flying will determine how far it flies in a set time, but as aphids can fly much longer than an hour or two, active flights of from between 7-12 hours have been recorded (Cockbain, 1961), this rather suggests that the aphids are making a “decision” to stop flying and descend from the jet stream. That said, in the words of the great C.G. Johnson “aphids are weak flyers”, they cannot make progress against headwinds of more than 2 km per hour (Johnson, 1954), although Trevor Lewis gives them slightly more power and suggests that the can navigate against winds of up to 3 km per hour (Lewis, 1964).

Whatever the upper limit is, it doesn’t mean that they are powerless when it comes to ‘deciding’ when to stop flying. In the words of Hugh Loxdale and colleagues, “aphids are not passive objects” (Loxdale et al, 1993). Aphidologists, were until the 1980s (Kennedy, 1986), generally somewhat sceptical about the ability of aphids to direct their flight in relation to specific host finding from the air and not just flying towards plants of the right colour (Kennedy et al., 1961), or at all after take-off (Haine, 1955). The general consensus now, is that aphids control the direction of their flight in the boundary layer*** but that it is determined by the wind at higher altitudes (Loxdale et al., 1993).   Whilst we are discussing viewpoints, another point of debate is on whether aphids migrate or not. Loxdale et al., (1993) state that “migration can be viewed ecologically as population redistribution through movement, regardless of whether deliberate of uncontrolled or from the behavioural viewpoint of a persistent straightened-out movement affected by the animal’s own locomotory exertions or by its active embarkation on a vehicle”. In the case of aphids the vehicle could be the wind. Under both definitions, aphids can be defined as undertaking migrations. Long-distance migration by aphids is defined as being greater than 20 km and short-distance (local) migration being less than this (Loxdale et al., 1993). Long-distance migration is likely to be the exception rather than the rule with most aphids making local flights and not venturing out of the boundary layer, sometimes travelling distances no more than a few hundred metres (Loxdale et al., 1993).

There are different types of winged aphids (morphs) and these show different angles of take-off and rates of climb.  In Aphis fabae for example, which host –alternates between spindle and bean, the gynoparae which migrate from the secondary host to the primary host, have a steeper angle of take-off and climb more rapidly than the alate exules which only disperse between the secondary host plants (David & Hardie, 1988).

Lost 4

http://influentialpoints.com/Images/Rhopalosiphum_padi_emigrant_alate_departing_from_primary_host_c2013-05-21_11-25-12ew.jpg

The gynoparae are thus much more likely to end up in the jet stream and be carried longer distances, with, of course, a greater chance of getting lost (Ward et al., 1998). The alate exules however, may only land in the next field or even in the same one, and easily find a new host plant (Loxdale et al., 1993). These differences between the morphs of host alternating aphids are also seen in the bird cherry-oat aphid Rhopalosiphum padi (Nottingham et al., 1991).  Once safely air-borne, the aphids then have another set of problems to overcome.

How do they ‘decide’ when to land? How do they ‘know’ that there are host plants below them? Aphids have two main senses that help them locate their host plants, vision and smell (odour recognition) (Kring, 1972; Döring, 2014). Generally speaking, aphids respond positively to what we perceive as green or yellow light and negatively to blue and red light (Döring & Chittka, 2007) although this is not an absolute rule. Some aphids are known to preferentially choose yellowing leaves (sign of previous infestation) e.g. Black Pecan Aphid Melanocallis caryaefoliae (Cottrell et al., 2009) which indicates a pretty sophisticated host finding suite of behaviours. Aphids in flight chambers will delay landing if presented with non-host odours even in the presence of a green target (Nottingham & Hardie, 1993) and conversely can be attracted to colourless water traps that have been scented with host plant odours (Chapman et al., 1981). Aphids are thus using both visual and olfactory cues to locate their host plants and to ‘decide’ when to descend from the jet stream or boundary layer (Kring, 1972; Döring, 2014). They are not merely aerial plankton, nor are they entirely at the mercy of the winds, they do not deserve to be described as passive (Reynolds & Reynolds, 2009).

Once at ground level and on a potential host plant, aphids go through a complicated suite of behaviours to determine if the host is suitable or not; if the plant meets all the required

Lost 5

From air to plant – how aphids chose their host plants – after Dixon (1973).

 

criteria, then the aphid will start feeding and reproducing. It is interesting to note that although there may be a lot of aphids in the air, the number of plants on the ground that

Lost 6

Settled safely and producing babies 🙂

http://beyondthehumaneye.blogspot.co.uk/2012/06/aphids.html  https://simonleather.files.wordpress.com/2016/04/cd0a4-aphidbirth2small.jpg

 

are infested with them is relatively low, about 10% in a diverse landscape (Staab et al., 2015), although in a crop, the level of infestation can approach 100% (e.g. Carter et al., 1980). The fact that in some cases less than 1% of those that set off will have found a host plant (Ward et al., 1998) is not a problem when you are a member of clone; as long as not all of the members of a clone gets lost the journey has been a success.

They may be small, they may be weak flyers, but enough of them find a suitable host plant to keep the clone alive and kicking; not all aphids get lost.

 

References

Carter, N., Mclean, I.F.G., Watt, A.D., & Dixon, A.F.G. (1980) Cereal aphids – a case study and review. Applied Biology, 5, 271-348.

Chapman, R.F., Bernays, E.A., & Simpson, S.J. (1981) Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. Journal of Chemical Ecology, 7, 881-888.

Cockbain, A.J. (1961) Fuel utilization and duration of tethered flight in Aphis fabae Scop. Journal of Experimental Biology, 38, 163-174.

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

David, C.T. & Hardie, J. (1988) The visual responses of free-flying summer and autumn forms of the black bean aphid, Aphis fabae, in an automated flight chamber. Physiological Entomology, 13, 277-284.

Dixon, A.F.G. (1971) Migration in aphids. Science Progress, Oxford, 59, 41-53.

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

Döring, T.F. & Chittka, L. (2007) Visual ecology of aphids – a classcial review on the role of colours in host finding. Arthropod-Plant Interactions, 1, 3-16.

Döring, T., Hardie, J., Leather, S.R., Spaethe, J., & Chittka, L. (2008) Can aphids play football? Antenna, 32, 146-147.

Döring, T. (2014) How aphids find their host plants, how they don’t. Annals of Applied Biology, 165, 3-26.

Elton, C.S. (1925) The dispersal of insects to Spitsbergen. Transactions of the Entomological Society of London, 73, 289-299.

Gislen, T. (1948) Aerial plankton and its conditions of life. Biological Reviews, 23, 109-126.

Haine, E. (1955) Aphid take-off in controlled wind speeds. Nature, 175, 474-475

Johnson, C.G. (1951) The study of wind-borne insect populations in relation to terrestrial ecology, flight periodicity and the estimation of aerial populations. Science Progress, 39, 41-62.

Johnson, C.G. (1954) Aphid migration in relation to weather. Biological Reviews, 29, 87-118

Kennedy, J. S., Booth, C. O. & Kershaw, W. J. S. (1961). Host finding by aphids in the field III Visual attraction. Annals of Applied Biology, 49, 1-21.

Kring, J.B. (1972) Flight behavior of aphids. Annual Review of Entomology, 17, 461-492.

Lewis, T. (1964) The effects of shelter on the distribution of insect pests. Scientific Horticulture, 17, 74-84

Loxdale, H. D., Hardie, J., Halbert, S., Foottit, R., Kidd, N. A. C. &Carter, C. I. (1993).The relative importance of short-range and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society, 68, 291-312.

Nottingham, S.F., Hardie, J. & Tatchell, G.M. (1991) Flight behaviour of the bird cherry aphid, Rhopalosiphum padi. Physiological Entomology, 16, 223-229.

Reynolds, A.M. & Reynolds, D.R. (2009)  Aphid aerial desnsity profiles are consistent with turbulent advection amplifying flight behaviours: abandoning the epithet ‘passive’. Proceedings of the Royal Society B, 276, 137-143.

Staab, M., Blüthgen, N., & Klein, A.M. (2015) Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment Oikos, 124, 827-834.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

 

Post script

Political and geographic borders are not factors that deter aphid migrants, Wiktelius (1984) points out that aphids regularly make the journey across the Baltic in both directions to and from Sweden.

Wiktelius, S. (1984) Long range migration of aphids into Sweden. International Journal of Biometeorology, 28, 185-200.

 

*Elton refers to it as North-East Land

** Johnson (1951) objects to this terminology in no uncertain terms. That said, as there are records of non-winged aphids being caught by aircraft (Kring, 1972), it does suggest that there may be some accidental migration going on.

*** The UK Met Office defines the boundary layer as “that part of the atmosphere that directly feels the effect of the earth’s surface” and goes on to say that depending on local conditions it can range in depth from a few metres to several kilometres.

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Ten papers that shook my world – Way & Banks (1964) – counting aphid eggs to protect crops

The previous papers in this series (Southwood, 1961; Haukioja & Niemelä 1976; Owen & Weigert, 1976), were all ones that had an influence on my post-PhD career. This one in contrast, had a direct effect on my PhD as well as on my subsequent career, and was, I guess, greatly influential in the publication of the first book to deal with the ecology of insect overwintering (Leather, Walters & Bale, 1993). In 1964 Mike Way, one of the early proponents of Integrated Pest Management (in fact considered to be the father of UK IPM), was working on control methods for the black bean aphid, Aphis fabae.

Bean aphids

Mike had recently joined Imperial College from Rothamsted Research Station where he had been leading research on ways to reduce pesticide use by farmers and growers.   During his time at Rothamsted he had worked closely with a colleague, C.J. Banks on the black bean aphid including studies on the overwintering eggs. As they said in the introduction to their paper, published four years after their experiments; “During the British winter A. fabae survives almost exclusively in the egg stage. Egg mortality might therefore be important in affecting size of populations of this species and in predicting outbreaks”. They investigated the effects of temperature and predators on the mortality of the eggs on the primary host, spindle, Euonymus europaeus, and concluded that the levels of mortality seen would not affect the success of the aphids the following spring. By 1968 (Way & Banks, 1968) they had followed up on the idea and began to feel confident that aphid populations on field beans could be predicted from the number of eggs on the winter host; spindle bushes. The publication of this paper stimulated the setting up of a long-term collaborative project monitoring Aphis fabae eggs on spindle bushes at over 300 locations throughout England south of the River Humber, and monitoring aphid numbers in about 100 bean fields per year.   In 1977 the results were finally published (Way et al., 1977) and the highly successful black bean aphid forecasting system was born. This was further refined by using the Rothamsted aphid suction trap data (Way et al., 1981).

This was also the year that I began my PhD at the University of East Anglia, working on the bird cherry-oat aphid, Rhopalosiphum padi. In the course of my preparatory reading I came across Way & Banks (1964) just in time to set up a plot of bird cherry saplings which I monitored for the next three winters, the first winter’s work resulting in my first publication (Leather, 1980). I subsequently went on to develop the bird cherry aphid forecasting system still used in Finland today (Leather & Lehti, 1981; Leather, 1983; Kurppa, 1989).

Finnish aphid forecasts

Sadly, despite the great success of these two systems there has not been a huge take-up of the idea, although the concept has been looked at for predicting pea aphid numbers in Sweden (Bommarco & Ekbom, 1995) and rosy apple aphids in Switzerland (Graf et al., 2006). Nevertheless, for me this paper was hugely influential and resulted in me counting aphid eggs for over 30 years!

References

Bommarco, R. & Ekbom, B. (1995) Phenology and prediction of pea aphid infestations on pas. International Journal of Pest Management, 41, 101-113

Graf, B., Höpli, H.U., Höhn, H. and Samietz, J. (2006) Temperature effects on egg development of the rosy apple aphid and forecasting of egg hatch. Entomologia Experimentalis et applicata, 119, 207-211

Haukioja, E. & Niemela, P. (1976) Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station, 13, 44-47.

Kurppa, S. (1989) Predicting outbreaks of Rhopalosiphum padi in Finland. Annales Agriculturae Fenniae 28: 333-348.

Leather, S. R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur Angewandte Entomolgie 96: 282-287.

Leather, S. R. & Lehti, J. P. (1981) Abundance and survival of eggs of the bird cherry-oat aphid, Rhopalosiphum padi in southern Finland. Annales entomologici Fennici 47;: 125-130.

Leather, S.R., Bale, J.S., & Walters, K.F.A. (1993) The Ecology of Insect Overwintering, First edn. Cambridge University Press, Cambridge.

Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492.

Southwood, T.R.E. (1961) The number of species of insect associated with various trees. Journal of Animal Ecology, 30, 1-8.

Way, M.J. & Banks, C.J. (1964) Natural mortality of eggs of the black bean aphid Aphis fabae on the spindle tree, Euonymus europaeus L. Annals of Applied Biology, 54, 255-267.

Way, M. J. & Banks, C. J. (1968). Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter Euonymus europaeus L. Annals of Applied Biology 62, 177-197.

Way, M. J., Cammel, M. E., Taylor, L. R. &Woiwod, I., P. (1981). The use of egg counts and suction trap samples to forecast the infestation of spring sown field beansVicia faba by the black bean aphid, Aphis fabae. Annals of Applied Biology 98: 21-34.

Way, M.J., Cammell, M.E., Alford, D.V., Gould, H.J., Graham, C.W., & Lane, A. (1977) Use of forecasting in chemical control of black bean aphid, Aphis fabae Scop., on spring-sown field beans, Vicia faba L. Plant Pathology, 26, 1-7.

 

Post script

Michael Way died in 2011 and is greatly missed by all those who knew him well. He examined my PhD thesis, and to my delight and relief, was very complimentary about it and passed it without the need for corrections. I was greatly honoured that a decade or so later I became one of his colleagues and worked alongside him at Silwood Park. He was a very modest and self-deprecating man and never had a bad word to say about anyone. He had a remarkable career, his first paper published in 1948 dealing the effect of DDT on bees (Way & Synge, 1948) and his last paper published in 2011 dealing with ants and biological control (Seguni et al., 2011), a remarkable 63 year span. His obituary can be found here http://www.telegraph.co.uk/news/obituaries/science-obituaries/8427667/Michael-Way.html

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