Tag Archives: phenological coincidence

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 😦

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