Opening and closing windows for herbivorous insects – Ten more papers that shook my world (Feeny, 1970)

For an insect, be it an herbivore, a predator or a parasite,  phenological coincidence is a matter of life or death   As autumn approaches and the days shorten, or depending on your physiology, the nights lengthen, the senescence feeders (White, 2015) come into their own, and aphids look forward to the increased flow of nitrogen in the phloem (Dixon, 1977). The flush feeders have long since passed their peak and readied themselves for winter, waiting as pupae, or hibernating larvae and adults, for the return of spring (Leather et al., 1993). Enough of the lyricism, on with the story. It is all about timing, or more technically, phenology.

As with many great concepts, the idea of a phenological window was based on good solid natural history.  Back in 1970 Paul Feeny, chemist* turned entomologist, published a landmark paper (Feeny, 1970) based on observations he had made during his PhD at the University of Oxford. Whilst wandering round Wytham Woods he had noticed that there were marked seasonal patterns in the number of lepidopteran species feeding on the oak trees, with more than half feeding in the spring (Feeny, 1966).

Most species of oak feeding Lepidoptera are spring feeders (from Feeny 1970).

Feeny wondered what was driving this very marked seasonal feeding pattern. Despite working closely with Varley and Gradwell, both very much in the natural enemy and weather drive insect population cycles camp (Varley, 1963; Varley & Gradwell, 1970), he suggested some alternative explanations, among them leaf toughness, which he measured using a ‘penetrometer’. He

Following in the great entomological tradition of homemade equipment – Feeny’s penetrometer (feeny, 1970).

also measured leaf water content, leaf nitrogen content, sugar and leaf tannins, all of which are characteristics of the host plant, i.e. bottom-up factors.  All his measurements showed that young leaves were much more suitable for winter moth larval growth and survival than the older leaves, in that nitrogen and leaf water content were higher in young leaves than

Mean larval and pupal weights of groups of 25 fourth-instar winter moth larvae reared on young and more mature oak leaves (data from Feeny, 1970).

old leaves, and young leaves were more tender than the older leaves.  He did not, however, consider leaf toughness to be the driving force selecting spring feeding, instead homing in, on what we know term host quality (Awmack & Leather, 2002), high nitrogen and leaf water content, coupled with lower levels of leaf tannins.  Although he did not use the term phenological coincidence in the paper it is clear from this paragraph that this is what he meant  “A high nitrogen content in young growing leaf tissue is, of course, expected and has been shown for many plants (e.g., Long 1961). Its coincidence in oak leaves with the main period of larval feeding is striking and supports the view that nitrogen content may be one of the most important factors governing early feeding”.

Influential though it was, two things struck me about Feeny’s paper, first, although the whole thrust of his argument is that oak plant chemistry is more suitable for lepidopteran larvae in the spring than later in the year, he makes no mention of the variation in timing of bud-burst that is, in oaks and many other trees, very obvious. Second, he appears to have overlooked the seminal paper by Paul Ehrlich and Peter Raven about the coevolution of secondary plant chemistry and host use by butterflies (Ehrlich & Raven 1964), now termed the coevolutionary arms race (Kareiva, 1999).

More recently, people have realised that coevolution of plant defences and herbivore utilisation is not just to do with plant chemistry, but also with the timing of budburst. Local populations of trees and the insects that feed on them ‘try’ to second guess egg hatch and budburst respectively, in the case of the tree to disrupt synchrony of herbivore egg hatch with peak budburst and vice versa in the case of the larvae (e.g. Tikkanen & Julkunen-Tiitto, 2003; Senior et al., 2020). The whole idea of phenological coincidence has now been renamed the phenological match hypothesis (Pearse et al., 2015).

The phenological match hypothesis can be summarised as follows:

1. Phenological coincidence – folivores and leaves emerge synchronously, thus, those leaves emerging at the population mean will experience the highest herbivore damage.
2. Folivores emerge first before the population mean of leaf set, so leaves that develop earlier will suffer more damage by folivores than those that emerge later.
3. Buds break before folivore egg hatch – early-season folivores emerge after the population mean of leaf set, by which time leaf defences are in place and the folivores can’t cope as shown by Feeny (1970).

Diagrammatic representation of the phenological match hypothesis (Pearse et al., 2015).

So now for the shaking my world bit. Despite being an academic grandchild of George Varley (he was my PhD supervisor’s supervisor) so coming from two generations of top-downers, I was, for many years an ardent advocate of the bottom-up school of insect population regulation.  I am now a little less biased against top-down effects, although as someone who works in crop protection and largely with herbivorous insects, I am more likely to look for solutions from the bottom-up :-).  Of course, my ideal solution is to use biological control coupled with plant resistance, thus marrying the two in perfect harmony as all good integrated pest managers aim to do**.

Oddly, even though as a PhD student, I photocopied most of Feeny’s papers, including conference proceedings and book chapters, I failed to cite a single one of them in my thesis.  When you consider that my whole thesis was pretty much based around the idea of phenological coincidence, (although like Feeny I did not use the term), this was a major omission on my part. Instead, influenced by Evelyn Pielou and her concept of seasonality, I invented a new word, seasonability*** to describe the concept (Leather, 1980).

“Seasonality has been defined as being synonymous with environmental variability (Pielou, 1975). In much the same way seasonability in aphids can be defined as the pre-programmed responses to predictable environmental changes, in other words, the aphid anticipates the trend in conditions”

If you work on aphids, the plant and its growth stage is pretty much everything that matters (Leather & Dixon, 1981) and if you work on an host-alternating aphid, this becomes even more important perhaps being one of, if not the major factor, driving the adoption of the host alternating life-cycle (Dixon, 1971).  My PhD work and most of what I have done since, is firmly based on the timing of events in insect life histories and their host plants,

The opening and closing of the phenological window for tree dwelling aphids (Dixon 1971).

be it programmed phenotypic response to changes in predictable changes in host nutritional quality in aphids (Wellings et al., 1980), to explaining why insects are pests in some environments and not others (Leather et al., 1989; Hicks et al., 2007). Despite the fact that the papers published from my

From my thesis (Leather, 1980) demonstrating a phenological window in wild grass host suitability for the bird cherry aphid when it needs to move from its woody host. Note my pretentious attempt to add yet more jargon to the aphid world – influx, reflux, what was I thinking! That said, note how it fills the gap on the graph above.

thesis were almost entirely based onthe effects of  host plant phenology on the growth and survival of aphids (e.g. Leather & Dixon, 1981, 1982) the word phenology is strikingly absent. I also note with some amusement, that over the years I seem to have been reluctant to use the term in the titles of papers.  Of the 218 papers that the Web of Science tells me I have authored, only five contain the word in their title (Leather, 2000; Bishop et al., 2013; Rowley et al., 2017, 2017; Senior et al., 2020). Of those I am senior author of only one, which leads me to wonder if have an unconscious bias against the word?

References

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

Bishop, T.R., Botham, M.S., Fox, R., Leather, S.R., Chapman, D.S. & Oliver, T.H. (2013) The utility of distribution data in predicting phenology. Methods in Ecology & Evolution, 4, 1024-1032.

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. (1977) Aphid Ecology: Life cycles, polymorphism, and population regulation. Annual Review of Ecology & Systematics, 8, 329-353.

Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants a study in coevolution. Evolution, 18, 586-608.

Feeny, P. P. 1966. Some effects on oak-feeding insects of seasonal changes in the nature of their food. Oxford D. Phil. thesis. Radcliffe Science Library, Oxford.

Feeny, P. (1970). Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology, 51, 565–581. 

Hicks, B.J., Aegerter, J.N., Leather, S.R. & Watt, A.D. (2007) Asynchrony in larval development of the pine beauty moth, Panolis flammea, on an introduced host plant may affect parasitoid efficacy. Arthropod-Plant Interactions, 1, 213-220.

Kareiva, P. (1999) Coevolutionary arms races: Is victory possible? Proceedings of the National Academy of Sciences USA, 96, 8-10.

Leather, S.R. (1980) Aspects of the Ecology of the Bird Cherry-Oat Aphid, Rhopalosiphum padi L.  PhD Thesis University of East Anglia, Norwich.

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.

Leather, S.R. & Dixon, A.F.G. (1982) Secondary host preferences and reproductive activity of the bird cherry-oat aphid, Rhopalosiphum padi. Annals of Applied Biology, 101, 219-228.

Leather, S.R. (2000) Herbivory, phenology, morphology and the expression of sex in trees: who is in the driver’s seat? Oikos, 90, 194-196.

Leather, S.R. & Dixon, A.F.G. (1982) Secondary host preferences and reproductive activity of the bird cherry-oat aphid, Rhopalosiphum padi. Annals of Applied Biology, 101, 219-228.

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.

Pearse, I.S., Funk, K.A., Kraft, T.S. & Koenig, W.D. (2015) Lagged effects of early-season herbivores on valley oak fecundity. Oecologia, 178, 361-368.

Pielou, E.C. (1975) Ecological Diversity, John Wiley & Sons Inc., New York.

Rowley, C., Cherrill, A., Leather, S.R. & Pope, T.W. (2017) Degree-day base phenological forecasting model of saddle gall midge (Halodiplosis marginata) (Diptera: Cecidomyiidae) emergence. Crop Protection, 102, 154-160.

Rowley, C., Cherrill, A., Leather, S.R., Nicholls, C., Ellis, S. & Pope, T. (2016) A review of the biology, ecology and control of saddle gall midge, Haplodiplosis marginata (Diptera: Cecidomyiidae) with a focus on phenological forecasting. Annals of Applied Biology, 169, 167-179.

Senior, V.L., Evans, L.C., Leather, S.R., Oliver, T.H. & Evans, K.L. (2020) Phenological responses in a sycamore-aphid-parasitoid system and consequences for aphid population dynamics; A 20 year case study. Global Change Biology, 26, 2814-2828.

Thompson, J.N. (1988) Coevolution and alternative hypotheses on insect/plant interactions. Ecology, 69, 893-895.

Tikkanen O-P. & Julkunen-Tiitto, R. (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia, 136, 244–251.

Varley, G.C. (1963) The interpretation of change and stability in insect populations. Proceedings of the Royal Society of Entomology Series C, 27, 52-57.

Varley, G.C. & Gradwell, G.R. (1970) Recent advances in insect population dynamics. Annual Review of Entomology, 15, 1-24.

Watt, A.D. & McFarlane, A. (1991) Winter moth on Sitka spruce: synchrony of egg hatch and budburst, and its effect on larval survival. Ecological Entomology, 16, 387-390.

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.

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

*Not many people realise that Paul Feeny’s first two degrees were in chemistry.

**unfortunately, the UK research councils don’t agree with me and despite several grant applications have bounced me every time. 😦

***it never caught on 😦

Ten more papers that shook my world – complex plant architecture provides more niches for insects – Lawton & Schroeder (1977)

Some years ago I wrote about how one of my ecological heroes, Sir Richard Southwood (later Lord Southwood), influenced my research and stimulated what has become a lifelong interest of mine, island biogeography, in particular the iconic species-area relationship. Apropos of this it seems apposite to write about another huge influence on my research, Sir John Lawton.  I first encountered John*, as he was then, at the tender age of 17, when our Sixth Form Science class were bussed from Ripon Grammar School to York University to hear a very enthusiastic arm-waving young ecologist, yes John Lawton, talking about food webs. Excellent as it was, it wasn’t, however, this talk that inspired me :-), but a paper that he and Dieter Schroeder wrote a few years later (Lawton & Schroeder, 1977), in which they showed that structurally more diverse plants potentially hosted more insect species per unit range than those plants with less complex architecture.  A couple of years later Strong & Levin (1979) showed that this also applied to fungal parasites in the USA.  The mechanism behind the finding was hypothesised to be based on apparency – the bigger you are the easier you are to find, the bigger you are, the more niches you can provide to be colonised, pretty much the same reasoning used to explain geographic island biogeography and species-area accumulation curves (Simberloff & Wilson, 1969). John Lawton, Don Strong and Sir Richard Southwood also highlighted this in their wonderful little book (Strong et al, 1984) which has provided excellent material for my lectures over the years.

As someone who is writing a book, theirs is an excellent example of how you can improve on other people’s offerings.  Staying with the theme of plant architectural complexity, Strong et al (1984) brilliantly reported on Vic Moran’s masterly study on the relationship between Opuntia growth forms and the number of insects associated with them (Moran, 1980).  Vic’s study was an advance on the previous studies because he examined one family of plants, rather than across families, so reducing the variance seen in other studies caused by phylogenetic effects. I should also point out that this paper was also an inspiration to me.

The figure as shown in Victor Moran’s paper.

The revamped Moran as shown in Strong & Lawton (1984).

Okay, so how did this shake my world? As I have mentioned before, my PhD and first two post-docs were on the bird cherry-oat aphid, Rhopalosiphum padi, a host-alternating aphid that uses bird cherry, Prunus padus, as its primary host.  Never being one to stick to one thing, I inevitably got interested in bird cherry in general and as well as eventually writing a paper about it (Leather, 1996) (my only publication in Journal of Ecology), I also, in due course, set up a long term experiment on it, the outcome of which I have written about previously. But, I digress, the first world shaking outcome of reading Lawton & Schroeder, was published in Ecological Entomology (incidentally edited by John Lawton at the time), in which I analysed the relationships between the insects associated with UK Prunus species and their distribution and evolutionary history, and showed that bird cherry had a depauperate insect fauna compared with other Prunus species (Leather, 1985).

I’m not working with very many points, but you get the picture (from Leather, 1985). Bird cherry (and also Gean, the common wild cherry. Prunus avium) hosts fewer insect species than would be expected from its range and history.

This in turn led me on to an even more ambitious project.  Inspired by a comment in Kennedy & Southwood (1984) that a better resolution of the species-plant range relationship would result if the analysis was done on a taxonomically restricted group of plants and by the comment in Southwood (1961) that the Rosaceae were a very special plant family, I spent several months wading through insect host lists to compile a data set of the insects associated with all the British Rosaceae.  Once analysed I submitted the results as two linked papers to the Journal of Animal Ecology.  Having responded to Southwood’s demand that “this manuscript be flensed of its too corpulent flesh” it was eventually published (Leather, 1996).  My somewhat pompous introduction to the paper is shown below.

“This relationship is modified by the structure or complexity of the plant, i.e. trees support more insect species than shrubs, which in turn support more species than herbs (Lawton & Schroder 1977; Strong & Levin 1979; Lawton 1983).”

“Kennedy & Southwood (1984) postulated that if taxonomically restricted groups of insects and/or plants were considered, the importance of many of these variables would increase. Few families of plants cover a sufficiently wide range of different growth forms ranging from small herbs to trees in large enough numbers to give statistically meaningful results. The Rosaceae are a notable exception and Southwood (1961) commented on the extraordinary number of insects associated with Rosaceous trees. It would thus appear that the Rosaceae and their associated insect fauna provide an unparalleled opportunity to test many of the current hypotheses put forward in recent years concerning insect host-plant relationships.”

Cutting the long story short (I am much better at flensing nowadays), I found  that Rosaceous trees had longer species lists than Rosaceous shrubs, which in turn had longer lists than herbaceous Rosaceae.

Rather messy, but does show that the more architecturally complex the plant, the more insect species it can potentially host (from Leather, 1986).

Flushed by the success of my Prunus based paper, I started to collect data on Finnish Macrolepidoptera feeding on Prunus to compare and contrast with my UK data (I can’t actually remember why this seemed a good idea).  Even if I say so myself, the results were intriguing (to me at any rate, the fact that only 19 people have cited it, would seem to suggest that others found it less so), in that host plant utilisation by the same species of Macrolepidoptera was different between island Britain and continental Finland (Leather, 1991).

 

 

From Leather (1991) Classic species-area graph from both countries but some intriguing differences in feeding specialisation.

Despite the less than impressive citation index for the UK-Finland comparison paper (Leather, 1991), I would like to extend the analysis to the whole of Europe, or at least to those countries that have comprehensive published distributions of their Flora.  I offer this as a project to our Entomology MSc students, every year, but so far, no luck ☹

Although only four of my papers can be directly attributed to the Lawton & Schroeder paper, and taking into account that the insect species richness of Rosacea paper, is number 13 in my all-time citation list, I feel justified in counting it as one of the papers that shook my World.

References

Kennedy, C.E.J. & Southwood, T.R.E. (1984) The number of species of insects associated with British trees: a re-analysis. Journal of Animal Ecology, 53, 455-478.

Lawton, J.H. & Schroder, D. (1977) Effects of plant type, size of geographical range and taxonomic isolation on numbers of insect species associated with British plants. Nature, 265, 137-140.

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. (1991) Feeding specialisation and host distribution of British and Finnish Prunus feeding macrolepidoptera. Oikos, 60, 40-48.

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

Moran, V.C. (1980) Interactions between phytophagous insects and their Opuntia hosts. Ecological Entomology, 5, 153-164.

Simberloff, D. & Wilson, E.O. (1969) Experimental zoogeography of islands: the colonization of empty islands. Ecology, 50, 278-296.

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

Strong, D.R. & Levin, D.A. (1979) Species richness of plant parasites and growth form of their hosts. American Naturalist, 114, 1-22.

Strong, D.R., Lawton, J.H. & Southwood, T.R.E. (1984) Insects on Plants – Community Patterns and Mechanisms. Blackwell Scientific Publication, Oxford.

 

*Many years later I worked with John when he was head of the Centre for Population Biology at Silwood Park.

 

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.

 

 

Ten more papers that shook my world – Plant growth formulae for entomologists – Radford (1967) and Wyatt & White (1977)

Plant growth formulae for entomologists, what a great title for a paper or even a book J These two papers, separated by a decade had a great influence on my PhD and subsequent entomological career, or at least the lab based part of it. I started my PhD at the University of East Anglia on October 2^nd 1977, where I was lucky enough to be supervised by that doyen of the aphid world, Professor Tony Dixon.  I was, and still am, convinced that the sooner you get started on practical work the better and that is what I tell my students.  Yes, reading is important but getting to know your organism early on, is just as, if not more, important. You can catch up on your in-depth reading later, but that early ‘hands on’ experience, even if what you first do is not publishable, is invaluable.  I see from my lab notebooks that my first experiments* were examining the effects of host plant on the fecundity and longevity of my study aphid, Rhopalosiphum padi.

My first experiment as a PhD student!

It was doing these very simple experiments, collecting development, survival and reproductive data that introduced me to the idea of measuring life history parameters in the round,

One of my first data sheets – not used in my thesis but gave me invaluable experience for later on.

rather than as single factors, akin to how ecologists move from measuring species diversity as a simple species count to using diversity indices that combine other attributes and describe the community more holistically. So it was with me and growth and reproductive rates. I wanted to be able to infer what my laboratory results might mean in the field and to develop faster methods of screening for host plant effects.  I came across, or was pointed in the direction of, two papers that had great influence on my research, Radford (1967)** about measuring growth rates, albeit of plants, and Wyatt & White (1977) on how to measure intrinsic rates of increase r_m without having to go through the very laborious and time-consuming methods devised by Birch (1948); working on aphids makes you do things in a hurry 😊

Ian Wyatt and his colleague Peter White did a series of painstaking laboratory experiments to obtain reproductive figures for aphids and mites and came up with a simplified version of the Birch equation such that

r_m = 0.738(lnM_d)/d

 where M_d = the number of offspring produced over a period of time equal to the pre-reproductive period D and 0.738 is a constant (Wyatt & Wyatt, 1977)

The Radford paper, reinforced by reading a paper by another great aphidologist, Helmut van Emden, Professor of Horticulture at the University of Reading (van Emden, 1969) convinced me that Mean Relative Growth Rate (MRGR) was the way to go to obtain comparative measures of host plant suitability for my aphids.  To save you looking it up, MRGR is calculated as follows:

The beauty of this, especially if you are working with very small animals such as aphids, is that you don’t need to weigh them at birth, you can if you want, just measure weights between two time periods.

Screening plants for resistance to aphids is an integral part of developing sustainable and environmentally friendly ways of protecting your crops.  At the time I started my PhD several methods were in use, ranging from measuring direct fecundity and developmental time (Dean, 1974), to short cuts such as counting the number of mature embryos at adult moult (Dewar, 1977) and of course Mean Relative Growth Rate (van Emden, 1969).  Although I tended to measure life-time fecundity and longevity for almost all my experiments, having the short cut of MRGR and in many cases the fecundity achieved in the first seven days of reproduction*** (e.g. Leather & Dixon, 1981) were useful tools to have.  What was the world shaking discovery for me, and something that in retrospect, I find surprising that no one else cottoned on to, was that MRGR was highly correlated with fecundity and that this meant that MRGR was correlated with the intrinsic rate of increase (Leather & Dixon, 1984).  This means that you can screen host plants and predict population trajectories with experimental observations that take less than half the time using the traditional measurements.  That paper proved very popular and is Number 7 in my citation list, with, at the time of writing, 80 citations.   A few years later, when I had moved on to working with other insect orders, I found that the relationship between MRGR and r_m applied to Lepidoptera and that different insect orders followed the same rules (Leather, 1994).

Lepidoptera and aphids, singing from the same data sheets (Leather, 1994).

So truly, a paper that shook my world.

References

Birch, L.C. (1948) The intrinsic rate of natural increase of an insect population.  Journal of Animal Ecology, 48, 15-26.

Dean, G.J.W. (1974) Effect of temperature on the cereal aphids, Metopolphium dirhodum (Wlk.), Rhoaplosiphum padi (L.) and Macrosiphum avenae (F.) (Hem., Aphididae).  Bulletin of Entomological Research, 63, 401-409.

Dewar, A.M. (1977) Assessment of methods for testing varietal resistance to aphids in cereals.  Annals of Applied Biology, 87, 183-190.

Fisher, R.A. (1921) Some remarks on the methods formulated in a recent article on ‘The quantitative analysis of plant growth’. Annals of Applied Biology, 7, 367-372.

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-oat aphid, Rhopalosihum padi.  Annals of Applied Biology, 97, 135-141.

Leather, S.R. & Dixon, A.F.G. (1984) Aphid growth and reproductive rates. Entomologia experimentalis et applicata, 35, 137-140.  80 cites number 7 in my list

Leather, S.R. (1994) Insect growth and reproductive rates. In Individuals, Populations and Patterns in Ecology (ed. by S.R. Leather, A.D. Watt, N.J. Mills & K.F.A. Walters), pp. 35-43. Intercept, Andover.

Radford, P.J. (1967) Growth analysis formulae – their use and abuse. Crop Science, 7, 171-175.

van Emden, H.F. (1969) Plant resistance to Myzus persicae induced by a plant regulator and measured by aphid relative growth rate. Entomologia experimentalis et applicata, 12, 125-131.

Wyatt, I. J. & White, P. F. (1977) Simple estimation of intrinsic increase rates for aphids and tetranychid mites. Journal of Applied Ecology 14, 757-766.

 

*

and boy was I quick off the mark.  I started my PhD on October 2nd and here I am 24 days later with cereal plants at GS 12 ready to receive aphids J

**

it is only fair to point out that Radford owed his inspiration to the work of that great statistician, Ronald Fisher (Fisher, 1921)

***

aphids like many insects produce over half their progeny in the first week or so

Ten more papers that shook my world – It pays to move away from home – Janzen (1970) & Connell (1971)

I have long held Dan Janzen in high regard, and not just because he wrote a paper with the memorable title “What are dandelions and aphids?”  (Janzen, 1977).  I have always found his writing enjoyable, and was, and still am, in awe of his ability to straddle whole swathes of ecology, both practically and conceptually. The paper that has, however, had the most impact on me, and perhaps the concept that Janzen is most renowned for, is the one that gave rise to the Janzen-Connell hypothesis/effect (Janzen, 1970).  Janzen was addressing the question of why tropical forests, while generally species rich, have a low density of adult trees of each species when compared with temperate forests (Black et al., 1950).  Janzen states “I believe that a third generalization is possible about tropical tree species as contrasted with temperate ones: for most species of lowland tropical trees, adults do not produce new adults in their immediate vicinity (where most seeds fall).”  He based this statement on his own personal observations, discussions with tropical foresters and on discussions with Joseph Connell.  He then works through several models testing different scenarios, from allelopathy*, different modes of seed dispersal and seed predation. Although allelopathy has been shown to affect seedling recruitment in several tree species (e.g. Webb et al., 1967), his conclusion was that the efficiency of seed/seedling specific predators was the main factor causing the patterns seen in tropical forest structure.  The simple take-home message, and one that I often say to the three of my grown-up sons who still live with us, is that it pays to move away from home; if your parents don’t kill you, then something else will 😊 Easy to remember and understand.

The Janzen model – the further away you are from your parent, the greater the probability that you will survive (Janzen, 1970).

The user-friendly version I use in lectures https://agoutienterprise.files.wordpress.com/2012/09/j-c-diagram1.jpg

So, given that the first mention in print is the Janzen 1970 paper, why is it the Janzen-Connell model/hypothesis/effect and why was a marine biologist,  Joseph Connell, writing about tropical forest diversity (Connell, 1971)?  It could so easily have been a repeat of the Wallace and Darwin contretemps. If you read both papers, it is obvious to see that both men had discusd the subject with each other, and saw their hypothesis as an extension of an earlier paper by the great ecologist, Robert Paine (Paine, 1966).  Connell refers to the Janzen paper as in press, but his ideas saw the light of day in 1970, albeit not analysed fully and referred to as in preparation, at a conference, the proceedings of which did not appear until the following year (Connell, 1971).  The actual data he referred to in his paper, did not appear in journal format until 1984, perhaps one of the longest in preps** ever (Connell et al., 1984).

Although Connell and Janzen continued to address the subject e.g. (Janzen, 1971; Connell, 1978), their names were not linked until Steve Hubbell did so in 1979 (Hubbell, 1979).  This linking of the two names seems to have been the fuse that set off the citation rocket.  As of now, it has been cited over 15 000 times and shows no signs of slowing down.

The Janzen-Connell citation rocket; 15 286 citations to date

So, apart from using it in teaching, how has the Janzen-Connell hypothesis shaken my world? Although I had used the concept in my teaching since the mid-1990s, it was my weekly walk round my 52 sycamore tree transect that got me thinking about it as research topic.  Field work is a great way to keep in touch with your study organism, things go one outside that don’t happen in the lab.  My sycamore transect was set up to monitor the insect herbivores and their natural enemies, but after a few years something else struck me, particularly, during high seed production years (another twenty-year data set for my never going to publish series).  I noticed that although lots of sycamore seedlings emerged underneath my study trees in the spring, by mid-summer hardly any were left; underneath other tree species, they were however, much more common, especially under oak trees.  My first thought was allelopathy, but a quick test using potted sycamore seedling in soil from underneath oak and sycamore trees with standard compost as a control, quickly showed this not to be the case.

Effects of soil type on growth of sycamore seedlings (F = 1.68 2/33 df P =NS).

I then used an undergraduate student assistant (paid I hasten to add) to do a couple of surveys, counting the incidence of sycamore seedlings and saplings underneath different tree species.  This convinced me that there was something going on and I set up twenty permanent plots in 2005, which I monitored until I left Silwood in 2012 (another set of data unlikely to be published), ten under mature sycamore and ten underneath mature oak trees, counting the number of sycamore seedlings that merged every spring and survived or not. After a couple of years I was convinced that there was every possibility of a Janzen-Connell effect going on and persuaded Alex Pigot, then a MSc student that it would be a great project.  To cut a long story short, Alex demonstrated that sycamore seedling survival, was as with tropical tree seedlings, dependent on predation pressure and that this was mainly due to invertebrate herbivores and was greatest underneath their parent trees.

Sycamore seedling mortality highest under sycamore and oak when exposed to invertebrates, vertebrates or both (Pigot & Leather, 2008).

Before anyone accuses me of taking credit for being the first person to demonstrate that the Janzen-Connell effect was also applicable to temperate forests, let me point you at a paper by Douglas Gill (Gill, 1975) who suggested that the spatial patterns of pines and oaks in the New Jersey Pine Barrens might be a result of differential seed predation as suggested by Janzen and Connell.

Despite the undoubted popularity of the Janzen-Connell Hypothesis in ecology, it is still not entirely clear cut; as my colleagues and I pointed out recently “What is clear, is that more studies targeting closed tall forests, and trees from other plant families and their seedlings are urgently needed before we can make sweeping conclusions about the generality of Janzen–Connell effects induced specifically by insects”  (Basett et al., 2019), but nevertheless this is a paper that shook my world and one that is definitely worth reading if you haven’t come across it before or just taken the concept it as gospel.

References

Basset, Y., Miller, S.E., Gripenberg, S., Ctvrtecka, R., Dahl, C., Leather, S.R. & Didham, R.K. (2019) An entomocentric view of the Janzen–Connell hypothesis. Insect Conservation and Diversity, 12, 1-8.

Black, G.A., Dobzhansky, T. & Pavan, C. (1950) Some attempts to estimate species diversity and population density of trees in Amazonian forests. Botanical Gazette, 111, 413-425.

Connell, J. H. (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and forest trees.  In: den Boer, P. J. and Gradwell, G. R. (eds), Dynamics of Populations. Centre for Agricultural Publications and Documentation, Wageningen, the Netherlands, pp. 298-312.

Connell, J.H. (1978) Diversity in tropical rain forests and coral reefs.  Science, 199, 1302-1310.

Connell, J.H., Tracey, J.G. & Webb, L.J. (1984) Compensatory recruitment, growth, and mortality as factors maintaining rain forest tree diversity. Ecological Monographs, 54, 141-164.

Gill, D.E.  (1975) Spatial patterning of pines and oaks in the New Jersey Pine Barrens. Journal of Ecology, 63, 291-298.

Hille Ris Lambers, J., Clark, J.S. & Beckage, B. (2002) Density-dependent mortality and the latitudinal gradient in species diversity. Nature, 417, 232-235.

Hubbell, S.P. (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science, 203, 1299-1309.

Janzen, D.H. (1970) Herbivores and the numbers of tree species in tropical forests. American Naturalist, 104, 501-528.

Janzen, D.H. (1971) Escape of juvenile Dioclea megacarpa (Leguminosae) vines from predators in a deciduous tropical forest. American Naturalist, 105, 97-112.

Janzen, D.H. (1977) What are dandelions and aphids? American Naturalist, 111, 586-589.

Paine, R.T. (1966) Food web complexity and species diversity.  American Naturalist, 100, 65-75.

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.

Webb, L.J., Tracey, J.G. & Haydock, K.P. (1967) A factor toxic to seedlings of the same species associated with living roots of the non-gregarious subtropical rain forest tree Grevillea robusta. Journal of Applied Ecology, 4, 13-25.

* the chemical inhibition of one plant (or other organism) by another, due to the release into the environment of substances acting as germination or growth inhibitors

**Let me know if you know of a longer one.  I don’t count Darwin, as he didn’t, as far as I know, actually refer to his theory in print before publication was forced upon him by Wallace.

Ten papers that shook my world – watching empty islands fill up – Simberloff & Wilson (1969)

Sadly this is the tenth and last in my series of the ten papers that had a great influence on my life as an ecologist.  I’m going to cheat somewhat and actually discuss three papers. In my defence they are extremely closely linked and I am pretty certain that in today’s publishing world they would all have had to have been combined anyway.  That aside, I really liked this experiment the first time I read about it and still rate it very highly.  I would, however, love to be able to travel back in time and give them a couple of hints with the benefit of hind-sight, although as the authors are two of the greatest living ecologists, Dan Simberloff and E O Wilson, I might be a bit apprehensive doing so 🙂 In any case, much of what I would have said was addressed a few years later (Simberloff, 1976).

Wilson and Simberloff wanted to practically test the island biogeography theory famously described by McArthur and Wilson a few year earlier (MacArthur & Wilson, 1967).  To do this they travelled to the Florida Keys and after due reconnaissance decided that the many mangrove “tree islands” would be ideal study sites (Figure 1).  Then came the really cool bit.

Figure 1.  Two of the experimental ‘islands’ from Wilson & Simberloff (1969)

They set about removing the arthropod animal life from nine of the islands (Figure 2), or as much as they could, by fogging with methyl bromide; not something we could do now.  They then monitored the islands at frequent intervals for the next year.  They had of course surveyed the islands before they fumigated them.

Figure 2.  What a cool project; defaunation in progress – from Wilson & Simberloff (1969)

Figure 3. Island equilibria – from Simberloff & Wilson (1970)

The major finding from their study was that recolonization happened quite quickly and that a year later had pretty much reached an equilibrium position (Figure 3).  Another important finding and one that has important implications for restoration and conservation strategies was that two years after the defaunation event, although the islands were well populated, the species composition, except for one island was less than 40% similar to the original inhabitants (Simberloff & Wilson (1970).  Most species present were new to those islands.  The analysis of the data presented in the two data papers is rather basic, some of the key island biogeographical premises are not addressed at all and I wondered why they had not done so.  Their data are all shown in some detail so it is possible to do some more analysis, which I took the liberty of doing.  The extra analysis shows why they did not discuss area effects per se .  The only significant relationship that I could find was that between the number of species and the distance from the ‘mainland’ source (Figure 4), which as predicted by MacArthur & Wilson (1967) was negative. Sadly, island size did not correlate with species number (Figure5).   Finally, there was a positive, but not significant relationship between the initial number of species found on an island and the number a year later (Figure 6).

Figure 4.  Relationship between distance from ‘mainland’ source and the number of arthropod species present (R² = 0.65, P <.0.05) Data from Simberloff & Wilson (1970).

Figure 5.  Island diameter and number of arthropod species (not statistically significant, r² = 0.19, although I am sure many politicians would view this as a positive trend). Data from Simberloff & Wilson (1970)

Figure 6.  Initial number of species on an island and number of species present one year later. Although it looks convincing (r² = 0.54), there are too few observations to reach statistical significance.  Data from Simberloff & Wilson (1970)

Although this work was extremely influential, (my Bracknell roundabouts study owes a lot to it), there were two major flaws in the original experimental design.  Firstly the number of islands was very low, but of course this is understandable, given the effort and complex logistics required to remove the arthropods safely (Figure 2).  The other flaw was that the islands did not cover a large enough range of sizes, thus making it less likely for the species-area pattern to be detected which was a great shame.

As I mentioned earlier, these short-comings were not ignored by the authors, and a few years later Sinberloff (1976) reported the results of an enhanced study, again in the Florida Keys, where he was able to convincingly demonstrate the species-area effect.   I guess that this was pretty satisfying as it tied up a number of loose strings.  He also managed to get the phrase “flogging a dead horse” into his introduction 🙂

Of the three papers, Simberloff & Wilson (1969) is the most highly cited (according to Google Scholar, 618 to date) and became a “citation classic”* in 1984 at which time it had accumulated 164 citations.  Simberloff & Wilson (1970) has attracted 252 cites with Wilson & Simberloff (1969) trailing in third with a mere 158 cites.  As a point of interest, Simberloff (1976) has so far received 313 cites.  To reiterate, the original mangrove island study, despite its flaws was a fantastic piece of work and Sinberloff and Wilson won the Mercer Award of the Ecological Society of America for this work in 1971.

I can think of no better person to explain why Simberloff & Wilson (1969) deserves its place in the Ecological Hall of Fame than Simberloff himself who in the commentary to the 1984 citation classic article wrote “I think the main reason it is cited, however, and its lasting contribution, is not so much that it supports the [equilibrium] theory, as that it reported a field experiment on ecological communities, and thus seemed dramatically different from the correlative approach that dominated this field”

 

References

MacArthur, R.H. & Wilson, E.O. (1967) The Theory of Island Biogeography Princeton University Press, Princeton.

Simberloff, D. (1976)  Experimental zoogeography of islands: effects of island size.  Ecology, 57, 629-648.

Simberloff, D. & Wilson, E.O. (1969) Experimental zoogeography of islands: the colonization of empty islands. Ecology, 50, 278-296.

Simberloff, D. & Wilson, E.O. (1970) Experimental zoogeography of islands: a two-year record of colonization. Ecology, 51, 934-937.

Wilson, E.O. & Simberloff, D. (1969) Experimental zoogeography of islands: defaunation and monitoring techniques. Ecology, 51, 267-278.

 

*Those of you who remember Current Contents will know what this means and here is the actual commentary.

Ten papers that shook my world – Solomon (1949) – quantifying predator efficiency

Solomon, M. E. (1949). The natural control of animal populations. Journal of Animal Ecology, 18, 1-35.*

 

According to Google Scholar there are 1149 (only 773 in 2013)citations to this paper, an average of 17.1 citations per year, compared with the 12.5 I reported back in 2013.  Although influential, it had a slow start, only 383 citations being recorded for it between 1949 and 1993. Since 2000 it has averaged about 48 citations a year (760 in total), 225 of those since 2013.** To the modern reader this paper comes across as wordy and discursive, more like a popular article than a scientific paper. This does not, however, mean that the science and the man behind the article were not first class. Journals had less pressure on their space in those days and scientists had more time to think and read. If only it were so now. Despite the relatively low number of citations, this paper has had an immense influence on the study of population dynamics, although I will have to confess, that for my generation who were undergraduates in the 1970s, Solomon’s little Study in Biology*** book, Population Dynamics, published in 1969, was our main, if not only, encounter with his work.

Making sure that nobody could claim my copy of Population Dynamics

Here Solomon introduces the term functional as in a density related response

Nowadays we remember the paper as the first one to formalise the term ‘functional response’ although the early citations to this paper are in reference to density dependence, competition, population regulation and population variability e.g. (Elton 1949; Glen 1954; Southwick 1955; Bakker 1963). Interestingly, one of the earlier papers to cite Solomon, (Burnett 1951) presented functional response curves but did not mention the term (Watt (1959)). To add further insult to injury, Holling (1959) in the same year, in his classic paper in which he described and numbered the types of functional responses did not even refer to Solomon, rather deferring to Watt’s paper (loc. cit.). Since then, with the likes of Varley, Gradwell and Hassell (1973) and luminaries such as Bob May (May 1978), this paper has been cited often, and justifiably, and continues to influence us to this day, including the author of this eulogy (Aqueel & Leather 2012). This paper as well as being  the first one to formalise the term ‘functional response’ was the first attempt to draw together the disparate conceptual strands of the first half of the twentieth century work on population dynamics in one coherent whole. Truly, a remarkable and very influential paper.

References

 

Aqueel, M. A., & Leather, S. R. (2012) Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids. Annals of Applied Biology, 160, 6-15.

Bakker, K. (1963) Backgrounds of controversies about population theories and their terminologies. Zeitschrift fur Angewandte Entomologie, 53, 187-208.

Burnett, T. (1951) Effects of temperature and host density on the rate of increase of an insect parasite. American Naturalist, 85, 337-352.

Elton, C. (1949) Population interspersion: an essay on animal community patterns. Journal of Ecology, 37, 1-25.

Glen, R. (1954) Factors that affect insect abundance. Journal of Economic Entomology, 47, 398-405.

Holling, C. S. (1959) Some characteristics of simple types of predation and parasitism. Canadian Entomologist, 91,385-398.

May, R. M. (1978) Host-parasitoid systems in patchy environments: A phenomenological model. Journal of Animal Ecology, 47, 833-844.

Solomon, M. E. (1969) Population Dynamics. Edward Arnold, London.

Southwick, C. H. (1955) The population dynamics of confined house mice supplied with unlimited food. Ecology, 36, 212-225.

Varley, G. C., Gradwell, G. R. & Hassell, M.P. (1973) Insect Population Ecology: An Analytical Approach. Blackwell Scientific Publications, Oxford.

Watt, K. E. F. (1959). A mathematical model for the effect of densities of attacked and attacking species on the numbers attacked. Canadian Entomologist, 91, 129-144.

 

Post script

A few months ago I was privileged to be given Robert Tillyard’s excellent The Insects of Australia and New Zealand (first published in 1926), by a former colleague of mine.

What made this even more special was that it had originally belonged to the great Maurice Solomon when he was a student, and contained some of his original annotations and revision notes.

 

Footnotes

*This is an expanded and updated version of the article I wrote as part of the British Ecological Society’s Centenary celebrations in 2013

**It is probably wishful thinking, but I might be tempted to think that by writing about this influential but somewhat overlooked paper, I increased the number of citations, so had a positive influence 🙂

***The Studies in Biology series, published by the then Institute of Biology (Now Royal Society of Biology), were excellent little books and the series on plant physiology were the main reason that I passed my first year plant physiology module as an undergraduate at Leeds University. I am reliably informed that there are plans to revive the series next year.

 

Ten papers that shook my world – Lewis (1969) – the importance of (h)edges for natural biological control

In 1969, Trevor Lewis, of what was then the Rothamsted Research Station (now Rothamsted Research), published two landmark papers (Lewis 1969ab). These papers, in which he described the importance of hedges as habitats for insects (Lewis, 1969a) and in acting as possible sources of natural enemies able to colonise nearby fields (Lewis, 1969b) were to have a profound effect on me and generations of applied entomologists and pest mangers to the present day.

In 1976 the UK experienced what is now recognised as the warmest year of the 20^th Century.  It was also the year that I started my final year as an undergraduate.  Before entering our final year we had to do a research placement or project.   I opted to do my project at home, I was making very good money as a temporary postman and as I usually finished my round by 10 am, I had plenty of time during the rest of the day to get to grips with my project.  I had come across the Lewis papers in lectures and thought that it would be interesting to do a similar study; given the weather I was also keen to spend as much time outside as possible 🙂 My Uncle James owned a local farm and was happy for me to sample some of his hawthorn hedges, so sampling hawthorn hedges was what I did during July and August of the glorious summer.

The intrepid student entomologist; trusty bike, clipboard and a copy of Chinery*. Note the wellington boots despite the heat 🙂

The hedges in question – three types of management

As I mentioned earlier, 1976 was the warmest year on record at the time, and I see from my report that during August I was recording temperatures in excess of 25^oC, even in the hedge bottoms.

The report

What is interesting is that although 1976 was one of the famous ladybird outbreak years (in fact last week I was interviewed by the BBC about my memories of that very same event) I didn’t record more than a handful of ladybirds in my surveys.  Perhaps inland Yorkshire just wasn’t attractive enough 🙂

Overall my results showed that over-clipping resulted in more crop pests being present and that hedges with less clipping supported a greater diversity of insect life than the more managed ones, very similar to results being reported today (e.g Amy et al., 2015).

Sadly, although Lewis’s two 1969 papers and to a certain extent his earlier paper in a much harder to access source (Lewis, 1964), led on to the concept of conservation headlands (Sotherton et al., 1989) and ‘crop islands’ (Thomas et al., 1991), which are an integral part of European Union subsidised farm payments, it was included in an influential review article (van Emden & Williams, 1974).  As pointed out recently by Terry McGlynn over at Small Pond Science, this often rings the death knell for a paper’s citation score.  As a result,  Lewis (1969b) has only been cited 91 times since 1969 and is barely remembered at all.   I remember being invited to be a facilitator at a Populations Under Pressure conference workshop on this very subject at the NERC Centre for Population Biology at Silwood Park about fifteen years ago and being surprised that none of the participants had even heard of Trevor Lewis let alone read his papers.

At the Populations Under Pressure conference brandishing my undergraduate hedgerow report!

The subject of hedgerow and crop edge management is still a highly important research area today, and you will be pleased to know that in the latest paper just submitted from my research group, we cite both of Trevor’s 1969 papers. Hopefully this will do something to redress the balance and bring Trevor some of the recognition that he deserves, however belated.

 

References

Amy, S.R., Heard, M.S., Hartley, S.E., George, C.T., Pywell, R.F. & Staley, J.T. (2015) Hedgerow rejuvenation management affects invertebrate communities through changes to habitat structure. Basic & Applied Ecology, 16: 443-451

Chinery, M. (1973) A Field Guide to the Insects of Britain and Northern Europe.  Collins, London

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

Lewis, T. (1969a). The distribution of flying insects near a low hedgerow. Journal of Applied Ecology 6: 443-452.

Lewis, T. (1969b). The diversity of the insect fauna in a hedgerow and neighbouring fields. Journal of Applied Ecology 6: 453-458.

Sotherton, N.W., Boatman, N.D. & Rands, M.R.W. (1989) The “Conservation Headland” experiment in cereal ecosystems. The Entomologist, 108: 135-143

Thomas, M.B., Wratten, S.D., & Sotherton, N.W. (1991) Creation of ‘island’ habitats in farmland to manipulate populations of beneficial arthropods: predator densities and emigration. Journal of Applied Ecology, 28: 906-917.

Van Emden, H.F. & Williams, G.F. (1974) Insect stability and diversity in agro-ecosystems. Annual Review of Entomology, 19: 455-475

*I still own that copy of Chinery which was a present for my 20^th birthday – take note of the date if anyone wants to send me a present or card 🙂

 

.

 

Ten Papers that shook my World – Root (1973) – When more means less – crop diversity reduces pest incidence

I can’t remember when I first read this paper but judging by the record card and the state of the actual hard copy of the paper, it was probably when I was doing my PhD in the late 1970s. This paper and its companion, which was published a year earlier* (Tahvanainen & Root, 1972), have had a significant effect on the scientific understanding and development of inter-cropping as a method of crop protection worldwide. Although inter-cropping in some form or another has been around a long time, the idea that it could be used as part of an integrated pest management programme was not proven.  In this landmark study, Root compared pure stands (plots) of collards (spring greens in the UK) (Brassica olercaea) with adjacent rows of collards grown intermingled with other herbaceous plants.  His premise being that it was well documented that pest outbreaks tend to be associated with pure monocultures of crops (Pimentel, 1961; Janzen, 1970) and he wished to test the hypothesis that natural enemies were more abundant and effective in vegetationally diverse areas  than in pure monocultures, the so-called ‘enemies hypothesis’.  This idea had been around a surprisingly long time e.g. Ullyett (1947) who remarked  “where weeds occur around headlands and in hedges, they should be left for the purpose of supporting parasites and predators important in the natural control of the diamond-back moth (Plutclla maculipennis Curt)”.  A decade later, Elton (1958,) refers to this statement, explaining that “these hedge rows form a reservoir for enemies and parasites of insects and mite pests of crops”.  I am not sure what it indicates but note that many groups around the world, including mine, are still working on this both at the local (field-scale) level (e.g. Ramsden et al., 2014) and landscape level (e.g. Rusch et al., 2013; Raymond et al., 2015).

Root explained the premise of the ‘enemies hypothesis’ as follows.  Predators and parasites are more effective at controlling herbivore populations in diverse habitats or plant communities because, diverse plant communities support a diversity of herbivores with a variety of phenologies, providing a steady supply of prey for the predators.  In addition, complex environments provide prey refugia, thus allowing the prey not to be completely eradicated.  Diverse plant communities also provide a broad range of additional resources for adult natural enemies e.g. pollen and nectar.

Root ran his experiment for three years and did indeed find a significant difference in herbivore load between the pure plots and the weedy rows, the former having a greater abundance of pests (mainly aphids and flea beetles) than the latter.

From Root (1973)

To his disappointment (I assume), he did not find any difference in the numbers of natural enemies between the two treatments. He thus had to come up with another idea to explain his results. His ingenious explanation is encapsulated in what he termed the Resource concentration hypothesis which states that herbivores are more likely to find and stay on hosts growing in dense or nearly pure stands and that the most specialised species often reach higher relative densities in simple environments.

Typical modern monocultures, beans, cabbages and wheat

He hypothesised that specialist herbivores were ‘trapped’ on the crop and accumulated whilst more generalist herbivores were able to and likely to move away from the crops to other host plants.  Root added that the ‘trapping effect’ of host patches depends on several factors such as stand size and purity.

In 1968, presumably as a result of what Root was discovering, Jorma Tahvanainen (one of the many great Finnish entomologists who appeared on the scene in the 1970s -, he retired in 2004) came to Cornell to do his PhD with Richard Root. Working on the same system and in the same meadow, Tahbanainen developed two new hypotheses to explain why more diverse cropping systems have fewer pest problems than monocultures. His experiments as he too found little evidence of natural enemies having an effect. He developed two new hypotheses, one he termed Associational resistance which I reproduce below exactly as published:

A natural community, such as a meadow, can be treated as a compound system composed of smaller, component communities (Root, 1973). The arthropods associated with different plant species represent important components in terrestrial systems. The available information indicates that the biotic, structural and microclimatic complexity of natural vegetation greatly ameliorates the herbivore pressure on these individual components, and consequently, on the system as a whole. Thus, it can be said that in a compound community there exists an “associational resistance” to herbivores in addition to the resistance of individual plant species. If the complex pattern of natural vegetation is broken down by growing plants in monocultures, most of this associational resistance is lost. As a result, specialized herbivores which are adapted to overcome the resistance of a particular plant species, and against which the associational resistance is most effective, can easily exploit the simplified system. Population outbreaks of such herbivores are thus more likely to occur in monocultures where their essential resources are highly concentrated

The other, is the Chemical Interference Hypothesis, in which he postulated that reduced herbivory in diverse communities due to chemical stimuli produced by non-host plants interfering with host finding or feeding behaviour of specialist herbivores.  His experimental set-up was very simple, but very effective.

How to send mixed signals to specialist herbivores – reproduced from Tahvanainen & Root (1972)

In simple terms, a monoculture sends out a very strong signal, it could be olfactory, e.g. a strong bouquet of crucifer volatiles, or for other herbivores it could be visual, or a combination of the two.

Conventional intensive agricultural landscape sending out strong ‘signals’ to specialist herbivores

Inter-cropping increases crop diversity and changes the crop ‘signal’ to one that now ‘confuses’ specialists. Note that I am not necessarily advocating a combined crop of wheat, beans and cabbages, as harvesting would be a nightmare 😉

 

The intercrop melange effect

These two papers have had a huge influence on the theory and practice of inter-cropping and agricultural diversification, although Root (1973) has had many more citations (1393 according to Web of Science on 11^th December 2015) than Tahvanainen & Root (1972) which has only had a meagre 429 citation to date.  The message coming out from the many studies that have now investigated the effect of intercropping crop diversification on pest abundance, is, that in general, polyculture is beneficial in terms of promoting biological control and that incorporating legumes into the system gives the best yield outcomes (Iverson et al,  2014).

Another take on intercropping that overcomes the potential problems of harvesting different crops from the same field, is the concept of planting different genotypes of the same species. Resistant plants tend to have fewer generalists present, although their individual yield may be reduced.  By planting a mixture of susceptible and resistant genotypes it is however, possible to have your cake and eat it, especially if it is not essential to have a single genotype crop.  This approach has been used to good effect in the production of short rotation willow coppice, where planting diverse genotypes of the same species reduces both pest and disease levels (Peacock et al., 2000, 2001).

Who would have that two simple field experiments conducted in an abandoned hay meadow outside Ithaca, New York almost fifty years ago would have such a far-reaching influence?

 

References

Elton, C. S. (1958) The Ecology of Invasions by Animals and Plants. London: Methuen & Co., Ltd. 159 pp.

Iverson, A. L., Makin, L. E., Ennis, K. K., Gonthier, D. J., Connor-Barrie, B. T., Remfret, J. L., Cardinale, B. J. &Perfecto, I. (2014). Do polycultures promote win-win or trade-offs in agricultural ecosystem services? A meta-analysis. Journal of Applied Ecology. 51, 1593-1602.

Peacock, L. & Herrick, S. (2000) Responses of the willow beetle Phratora vulgatissima to genetically and spatially diverse Salix spp. plantations. Journal of Applied Ecology, 37, 821-831.

Peacock, L., Hunter, T., Turner, H., & Brain, P. (2001) Does host genotype diversity affect the distribution of insect and disease in willow cropping systems? Journal of Applied Ecology, 38, 1070-1081

Janzen, D.H. (1970) The unexploited tropics.  Bulletin of the Ecological Society of America, 51, 4-7

Pimentel, D. (1961). Species diversity and insect population outbreaks. Annals of the Entomological Society of America, 54, 76-86.

Ramsden, M. W., Menéndez, R., Leather, S. R. & Wackers, F. (2014). Optimizing field margins for biocontrol services: the relative roles of aphid abundance, annual floral resource, and overwinter habitat in enhancing aphid natural enemies. Agriculture Ecosystems and Environment, 199, 94-104.

Raymond, L., Ortiz-Martinez, S. A. &Lavandero, B. (2015). Temporal variability of aphid biological control in contrasting landscape contexts. Biological Control , 90, 148-156.

Root, R. B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards. Ecological Monographs, 43, 95-124.  1393 citations

Rusch, A., Bommarco, R., Jonsson, M., Smith, H. G. &Ekbom, B. (2013). Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. Journal of Applied Ecology, 50, 345-354.

Tahvanainen, J. & Root, R. B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia, 10, 321-346. 429 citations

Ullyett, G. C. (1947) Mortality factors in populations of Plutella maculipennis Curtis (Tineidae: Lep.) and their relation to the problem of control. Union of South Africa, Department of Agriculture and Forestry, Entomology Memoirs, 2, 77-202.

Post script

*I suspect, judging by how the two papers cite each other, that the Root (1973) paper was actually submitted first but that the vagaries of the publication system ,  meant that follow-up paper, Tahvanainen & Root (1972) appeared first.

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.

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).

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