Tag Archives: cereals

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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Ten more papers that shook my world – When it comes to plant-insect interactions its growth stage, not age that counts Watt (1979)

This is not just about a paper, but also about mentoring!  At the beginning of October 1977, I hesitantly knocked on the door of Professor Tony Dixon’s outer office in the School of Biological Sciences at the University of East Anglia, Norwich.  Tony was to become my PhD supervisor for the next three years and my friend and colleague for the next forty plus years, but until that day I had never met him, as my interview had been conducted entirely by telephone and in those pre-internet days, unless you had met someone at a conference you really only knew them by their papers and reputation.  I knew Tony because of his great little book, The Biology of Aphids which I had bought as an undergraduate in 1975, when I realised that aphids were really cool 😊 I told his secretary who I was and she directed me through to his office.  Tony looked up, said hello and asking me to follow him, took me down to the lab where I was to spend the next three years and introduced me to a tall, moustachioed Scotsman, Allan Watt, whom I was later to discover had a wicked sense of humour, and was to become not just a colleague and collaborator, but also a great friend, a friendship that continues to this day.  Tony’s introduction was roughly along the lines of “This is Allan, he’ll tell you what to do” and he did. Allan was just starting the final year of his PhD which was, like a number of us in Tony’s lab, on cereal aphids, in Allan’s case Sitobion avenae and Metopolphium dirhodum, the two major pests of cereals in the UK at the time.  My PhD was on a less abundant (in cereal crops), but equally problematic aphid, due to its ability to transmit Barley Yellow Dwarf Virus, the bird cherry-oat aphid Rhopalosiphum padi.  Having got my aphid cultures set up and done a couple of practice mini-experiments, I asked Allan what he was doing with his aphids.  He told me that he was looking at the effect of cereal growth stage on the survival and reproduction of his two aphid species and that the age of the plant had a significant effect on the aphids and that this varied between the two species, which he published a couple of years later (Watt, 1979).  Having been immersed in the cereal aphid literature for a couple of months, I knew that no one had done this for my aphid, and even then, being a great believer in “standing on the shoulders of giants” I figured that I could do the same for my aphid, but, in that never ending treadmill of adding novelty, also look at the effect of feeding position*. Allan’s advice and help stood me in good stead, and in due course I successfully published the results of my experiment (Leather & Dixon, 1981).

So, leaving aside me getting a publication as a result of Allan’s paper, how did this shake my World?  Well, first of all, it really drove home to me that plant phenological stage was incredibly important for insect-plant interactions and that unless you know the precise growth stage at which an interaction is happening it is difficult to compare other peoples’ results to yours and each other’s. As a result, it has led me as a reviewer and reader of papers, to be very scathing of phrases such as “ten-day old wheat plant”, “week old cabbage seedlings”, “young pea plant” (Leather, 2010).  It is deeply unhelpful for anyone wanting to repeat or compare similar work.  Just a few degrees difference in temperature over a week can move a plant from one phenological stage to another. There is no excuse for this type of sloppiness.

Two seven-day old wheat plants, same cultivar, same germination date, one reared at 20⁰C the other at 10⁰C. Growth stage 12 versus Growth stage 10 (Growth stages as described by Tottman & Makepeace, 1979).

The same two plants now fourteen day sold, GS 13 versus GS 12

It is not hard to find a solution.  The World has been blessed by the invention of the BBCH** system for coding plant phenological stages (Meier et al., 2009).  This system, which now exists for most major crop plants, including trees, means that there is no excuse for anyone to ever use the phrase “ten-day old plant” or similar wording. If by some chance, your plant does not yet have a BBCH description, either describe the growth stage that your plants are at in very precise terms or take the time to codify it yourself and submit it to a journal such as Annals of Applied Biology which has a long history of publishing such articles.

To be fair, before the BBCH system came into being, people had published descriptions of plant growth stages for some of the major crops, e.g. cereals (Feekes, 1941; Large, 1954), but they were not standardised, and in some cases, too broad-brush.  The stimulus for a standardised, decimal system of coding plant phenological stages was the publication of the Zadoks scale for cereals (Zadoks et al., 1974) and the illustrated follow-up a few years later (Tottman & Makepeace, 1979), the latter being the blueprint on which phenological growth stage papers are now based.

I look forward to the day when authors understand that a precise knowledge of plant growth stage is essential to understanding insect-plant interactions and I do NOT have to chide authors for not using the BBCH codification when I review their papers.

 

References

Feekes, W. (1941) De Tarwe en haar milieu. Vers. XVII Tech. Tarwe Comm. Groningen, 560-561.

Large, E.C. (1954) Growth stages in cereals. Plant Pathology, 3, 128-129.

Leather, S.R. (2010) Precise knowledge of plant growth stages enhances applied and pure research. Annals of Applied Biology, 157, 159-161.

Leather, S.R. & Dixon, A.F.G. (1981) The effect of cereal growth stage and feeding site on the reproductive activity of the bird cherry aphid Rhopalosiphum padi. Annals of Applied  Biology, 97, 135-141.

Meier, U., Bleiholder, H., Buhr, L., Feller, C., Hack, H., Hess, M., Lancashire, P.D., Schnock, U., Strauss, R., Vanden Boom, T., Weber, E. & Zwerger, P. (2009) The BBCH system to coding the phenological growth stages of plants – history and publications. Journal fur Kulturpflanzen, 61, S.41-52.

Tottman, D.R. & Makepeace, R.J. (1979) An explanation of the decimal code for the growth stage of cereals, with illustrations. Annals of Applied Biology, 93, 221-234.

Watt, A.D. (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolphium dirhodum. Annals of Applied Biology, 91, 147-157.

Watt, A.D. & Dixon, A.F.G. (1981) The effect of cereal growth stages and crowding of aphids on the induction of alatae in Sitobion avenae. Ecological Entomology, 6, 441-447.

Watt, A.D. & Wratten, S.D. (1984) The effects of growth stage in wheat on yield reductions caused by the rose grain aphid, Metopolophium dirhodum. Annals of Applied Biology, 104, 393-397.

Zadoks, J.C., Chang, T.T. & Konzak, C.F. (1974) A decimal code for the growth stages of cereals. Weed Research, 14, 415-421.

 

 

 

*

*Rhopaloisphum padi, in contrast to Sitobion avenae, is usually found on the lower stem and leaves of cereals.

**

The abbreviation BBCH derives from the names of the originally participating stakeholders: “Biologische Bundesanstalt, Bundessortenamt und CHemische Industrie”. Allegedly, the abbreviation is said to unofficially represent the four companies that initially sponsored its development; Bayer, BASF, Ciba-Geigy, and Hoechst.

 

 

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Not all aphids live on leaves

I haven’t written about aphids for a while, so I thought I would indulge myself and tell you about a few of my favourite aphids.  Most people’s perceptions of aphids (assuming that they know what  aphids are of course) is that they live on leaves.  They will I think, also possibly know that they are usually found on the undersides of leaves, although I may be assuming too much here.  In fact, many species of aphid do not live on leaves; a number of species feed on shoots, twigs and branches and some actually feed on the main trunks of trees.  Yet other species live on the roots of trees and herbaceous plants, such as the apple-grass aphid, Rhopalosiphum insertum which can be a pest of apples and cereals, feeding on the leaves and buds of apples and the roots of grasses and cereals.   Another root-feeding aphid that is a double pest, is Pachypappa tremulae, the spruce root aphid, which host alternates between the aerial parts of aspen trees and the roots of Norway spruce; easily visible when infesting the roots of young potted plants due to the presence of white waxy tufts on its rear end.

Some aphids not only live underground feeding on roots, but are entirely dependent on being farmed by ants e.g.  Tetraneura ulmi, which host-alternates between elm and grass roots, and  Forda formicaria, which host-alternates between Pistachio trees and grass roots.

Forda_formicaria_hirsuta_root_aphid_03-03-13_3

http://www.aphotofauna.com/images/bugs_homoptera/bug_forda_formicaria_hirsuta_root_aphid_03-03-13_3.jpg

Both these aphids are looked after or ‘farmed’ by the yellow meadow ant Lasius flavus in exchange for donations of honeydew.

Lasius%20flavus%202

These two aphid species, along with a number of others, have an enlarged anal plate surrounded by special hairs that form the so-called trophobiotic organ.  This acts as a storage device that allows the aphid to accumulate honeydew ready for the ants to remove.  Those aphids that have a more casual (facultative) relationship with ants, do not have this organ which is the basis of this remarkable mutualism.

Another aphid that is farmed by ants, but in a somewhat different way, is the rather larger rose root aphid, Maculolachnus submacaula, which as its name suggests, feeds on rose roots.  In this case, the ants allow the aphids above ground but only in an ant tunnel, similar to those produced by termites when they are infesting a building.  I have only ever been lucky enough to see this aphid once, some 35 years ago in Norwich when I was doing my PhD and noticed things that looked like termite trails running up the main stem of one of my rose bushes.  On breaking them open, well I am a curious entomologist, I found to my surprise not only ants but large brown aphids.

Maculolachnus submacula nest

http://jardiweb-floralbum.forumsactifs.com/t1797-colonie-de-pucerons

for a better view of the aphid see http://www.afripics.co.za/home/products/product.php?ProductID=1301564582

But of course the really spectacular ones are those that feed on branches of trees such as the giant willow aphid Tuberolachnus salignus (famous for its sharks fin) and those from the genus Stomaphis which feed through the bark of trees such as oak and

Tuberolachnus

sycamore and are possessed of truly enormous mouthparts such as those of Stomaphis aceris which feeds on sycamore

Stomaphis query aceris

This one, despite its enormous mouthparts, is quite difficult to find as it hides underneath the bark, but luckily it is ant attended so if you see ants scurrying around on the bark of sycamore and disappearing underneath loose flaking bits, it is a good bet that if you gently lever off the loose bark you will find yourself in the presence of this weird-looking creature.

The more I learn about aphids the more I find to marvel at.  Aphids really are remarkable and we know so little about so many of them and their weird and wonderful life styles.

Useful References

Blackman, R.L. & Eastop, V.F. (19 94) Aphids on the World’s TreesAn  Identification and Information Guide.  CABI Publishing. http://www.aphidsonworldsplants.info/index.htm

Evenhuis, H.H. (1968)  The natural control of the apple grass aphid,  Rhopalosiphum insertum, with remarks on the control of apple aphids in general in The Netherlands. Netherlands Journal of Plant Pathology, 74, 106-117  http://link.springer.com/article/10.1007/BF02309501#page-1

Farrell, J.A. & Stufkens, M.W. (1989) Flight activity and cereal host relationships of Rhopalosiphum spp. (Homoptera: Aphididae) in Canterbury New Zealand Journal of Journal of Crop and Horticultural Science, 17, 1-7  http://www.tandfonline.com/doi/abs/10.1080/01140671.1989.10428003

Ivens, A.B.F., Kronauer, D.J.C., Pen, I., Weissing, F.J. & Boomsma, J.J. (2012)  Ants farm subterranean aphids mostly in single clone groups – an example of prudent husbandry for carbohydrates and proteins?  BMC Evolutionary Biology, 12:106 http://link.springer.com/article/10.1186%2F1471-2148-12-106

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