I’ll start with a question. What do Lady’s Mantle, Great Burnet, Agrimony, Mountain Avens, Cotoneaster, cinquefolil (Potentilla), strawberries, raspberries, cherries, sloes, apples, rowans and almonds all have in common? The answer may come as a surprise to many; they are all members of the Rose family. This may shcok some of you, but I don’t have a great deal of time for the domesticate hybrid tea roses so common in many gardens.
Hybrid tea rose – looking nothing like the real roses
I think they’re vastly overrated and as many varieties do not produce pollen or nectar as far as insects are concerned they are a waste of space. My experience of working on members of the Rosaceae arose as a by-product of working on the bird cherry-oat aphid, the primary host of which is the bird cherry, Prunus padus (Leather & Dixon, 1981), and the bird cherry ermine moth, Ypomeuta evonymellus which specialises on the bird cherry (Leather & Lehti, 1982). Strangely, it was my interest in island biogeography, in particular the species-area relationship, that got me hooked on the Rosaceae. I had noticed while sampling bird cherry trees that relatively few insects attacked them, and so wondered if they were special in some way compared with other species of Prunus, and sure enough using host plant records, they did seem to be less insect friendly than their congeners (Leather, 1985). Having got hooked on counting dots on plant distribution maps and realising that the Rosaceae would be a great plant family to test the idea that the species-area relationship would be improved by confining it to a single family (Kennedy & Southwood, 1984), I embarked on a marathon dot counting and host plant record seeking quest (Leather, 1986).
For the paper, I restricted my analysis to the 59 species that Perrings & Walter (1962) listed as native or naturalised to the British Isles, but there are of course many more members of the Rosaceae than that to be found in Britain. They are an extremely important plant family both economically and horticulturally speaking, with over 2500 species in 90 genera to choose from (Sytsma, 2016). The Rose family is divided into four subfamilies based primarily on their fruit. The Amygdaloideae, those species characterised by the possession of fleshy stone fruits, almonds, cherries, peaches, plums etc. The Maloideae, trees with pomes, fruits in which the floral hypanthium becomes fleshy, e.g apples and pears. The Rosoideae, which includes species such as roses, and burnets, with dry fruits that do not open (achenes), and the brambles, raspberries and strawberries, which have drupelets, small, aggregated drupes, and finally the Spiraeoideae, species with dry fruits that open on one side (follicles) e.g Spirea, Physocarpus).
To me, however, the thing that makes a rose a rose, is the flower. Typically, rose flowers have five sepals which are easier to see before the flowers open and five petals, although there are always some exceptions; for example, Mountain
Sepals for the uninitiated; luckily I have a rose bush that seems to be able to flower all the year round (this picture taken October 28th)
Avens, Dryas octopetala, which as the name tells us, has eight petals but still manages to have that rose ‘look’.
As you might expect from a family that has produced the much loved (but not by me) hybrid tea roses, not all the flowers are white, even within the same species, brambles for example, range from the ‘normal’ white to rich
Pink hedgerow brambles, Sutton, Shropshire September 2020.
pinks, and many of the herbaceous members have bright yellow (e.g. Agrimony and Wood Avens) or orange (e.g Water Avens) flowers.
Delicate herbaceous plants with white and yellow flowers.
White flowers do, however, seem to be the rule in the woodier members of
Shrubby bushes with white flowers.
the family, although pink shading is not uncommon.
The ways in which the flowers are presented can also vary between species, single flowers being the exception rather than the rule.
Cloudbursts (corymbiform panicle), racemes and compound cymes, but still roses. Fun fact, Meadowseet, Filipendulal ulmaria, is rich in salicylic acid and can be used to cure headaches.
I hope you’ve enjoyed this ramble through the roses as much as me, but finally, as an entomologist, it would be remiss of me not to point you at one or two spectacular examples of insect-rose interactions.
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.
If you are interested in how appearance dates for UK butterfly species have changed since 1976, then here are the data
Most people have heard about sloe gin, but have you ever tried salt-fermented sloes? Here is a recipe from Jeff Ollerton, perhaps better known as a pollinator ecologist, but also not afraid to think outside the box J
If you were in the European silkworm business two or three hundred years ago the last thing you wanted to find in your colony were stiff dead caterpillars. Worse still would be if when you picked them up and bent them, they snapped in half and revealed a solid white or green interior, giving them the appearance of a stick of chalk. Horror stricken you realise that your beloved silkworms have been struck down by white or green muscardine disease, or if you were an Italian, calcino; in both cases the name refers to the chalk like appearance of the inside of the stricken larvae. By the middle of the 19th century the combined effects of the industrial revolution, the revival of the Japanese silk industry and an epidemic of viral and fungal diseases had pretty much shut down the European silk industry (Federico, 1997). We now know that the muscardine diseases are caused by the entompathogenic fungi Beauveria bassiana and Metarhizium anisipoliae, although this was not realised until the early part of the 19th Century when the Italian naturalist Agostino Bassi discovered their true nature.
So what about the aphids I hear you asking? I have written earlier about the attacks that aphids have to suffer from predators and parasitoids, but that is not all with which they have to contend. Fungal diseases (Dean &Wilding, 1973; Rabasse et al., 1982; Aqueel & Leather, 2013) also attack aphids in the same way that they attack most other insects. In the case of aphids, it is not one of the muscardines, instead they are attacked by a number of fungi belonging to the Entomophthoraceae. The first member of this family to be recognised as a fungus was named Empusa musca (now Entomophthora muscae) by Charles de Geer in 1782 (Cohn, 1855). As the name suggests, it attacks house flies. There are, however, a number of different entomopathogenic fungi that specialise in attacking aphids, Erynia neoaphidis, and other members of the Entomophtoraceae, being the most commonly seen (Dean & Wilding,
An aphid unfortunate enough to encounter an insect infecting fungal spore and lacking the appropriate symbionts (Parker et al., 2013) is very likely to suffer a slow and lingering death as the fungal mycelia proliferate within its body.
Pandora neoaphidis infected pea aphids (photo Tom Pope)
On landing on a susceptible aphid, the fungal spore germinates and the germ tube penetrates the aphid, either directly through the cuticle or via a nearby spiracle. Unlike those other invidious invaders of aphids, the parasitoids, entomopathogenic fungi need very specific environmental conditions to successfully colonise their aphid hosts. The damper the better, and if the aphid is surrounded by liquid water the more likely the fungus is to be able to effect an entry (Wilding, 1969; Dean & Wilding, 1973). More than a century ago Paul Hayhurst of Harvard University noticed that galls of the Chenopodium aphid, Hayhurstia atriplicis (then known as Aphis atriplicis) that were ruptured and had allowed water in, had a much higher incidence of diseased aphids than the intact galls (Hayhurst, 1909). Another more recent indication of this dependence on damp conditions is a mention of a high incidence of Pandora neoaphidis (described as Empusa aphidis) on Schizolachnus pini-radiatae being associated with higher than average rainfall (Grobler, 1962).
The earliest experiment involving aphid specific entompathogenic fungi that I have been able to find is from the latter half of the 19th Century (Houghton & Phillips, 1885).
“I placed some infected aphides under a glass with healthy specimens from my garden-beans and in a short time these became similarly covered with the same red-coloured fungoid growth. The n*****s took the scarlet fever and died.”
Their conclusion was that it was an Entomopthora species, perhaps related to, if not, E. planchoniana.
Although fungal pathogens have been shown to be able to reduce aphid populations in the field (Fluke*, 1925; Grobler et al., 1962; Plantegenest et al., 2001), their effectiveness as biological control agents on their own is variable and unpredictable (Milner, 1997). Most often, they are used either as biopesticides, or in conjunction with parasitoids and predators (e.g. Milner, 1997; Aqueel & Leather, 2013). One of the problems that entompathogenic fungi have is ‘finding’ their hosts. While it is known that entompathogenic fungi, as with entomopathogenic viruses, affect the behaviour of many insect that they attack (Hughes et al., 2011), by making them move to locations on their host plant where they are more likely to infect their kin, as far as I know, there is only one record of this for aphids (Harper, 1958). Surely a productive avenue of research to follow? That said, these clever fungi have another option up their mycelial sleeves. They are, like other fungi, able to discharge their spores explosively. Erynia neopahidis can project its spores more than 3mm vertically and more than 5 mm horizontally (Hemmati et al., 2001). This may seem a tiny distance to you and me, but the spores only need to get further than 2 mm to get air borne and move on to other plants or plant parts. It might be a leap into the unknown but it seems to work out all right for the fungi 🙂
Aqueel, M.A. & Leather, S.R. (2013) Virulence of Verticillium lecanii (Z.) against cereal aphids; does timing of infection affect the performance of parasitoids and predators? Pest Management Science,69, 493-498.
Cohn, F. (1855) Empusa muscae und die Krankeit der Stubenfliegen Nova acta Academiae
Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum, 25, 301-360
Hughes, D.P., Andersen, S.B., Hywel-Jones, N.L. , Himaman, W., Billen, J. & Boomsma, J. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology,11, 13.
Plantegenest, M., Pierre, J.S., Dedryver, C.A. & Kindlmann, P. (2001) Assessment of the relative impact of different natural enemies on population dynamics of the grain aphid Sitobion avenae in the field. Ecological Entomology,26, 404-410.
Rabasse, J.M., Dedryver, C.A., Molionari, J. & Lafont, J.P. (1982) Facteurs de limitation des populations d’Aphis fabae dans l’Ouest de la France 4. Nouvelles donnees sur le deroulement des epizooties entomophtoracees sur feverole de printemps. Entomophaga,27, 39-53.
Roditakis, E., Couzin, J.D., K., B., Franks, N.R. & Charnley, R.K. (2000) Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour. Annals of Applied Biology,137, 329-335.
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:
Phenological coincidence – folivores and leaves emerge synchronously, thus, those leaves emerging at the population mean will experience the highest herbivore damage.
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.
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?
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.
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.
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., 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.