The most difficult thing I have ever had to write – Insects – A Very Short Introduction

The book!

I have written a lot of papers (more than 220 according to Web of Science) and quite a few books, two real ones (Leather et al., 1993; Leather & Bland, 1996) and eight edited volumes, over the last forty odd years. Up until now I thought the most exacting piece of writing I had ever done was my entry for the Biological Flora (Leather, 1996).  I mention this because it has a very similar feel to my most recent, most difficult piece of writing, Insects, A Very Short Introduction.

I did my PhD on the bird cherry aphid, Rhopalosiphum padi (Leather, 1980) during which I developed a real love for the bird cherry tree, Prunus padus. Just to illustrate this, my second son’s middle name is Tuomi – Finnish for bird cherry. Over the next decade or so I expanded my studies on to the different insects associated with it and also became quite adept at striking scions, grafting it and manipulating its phenology. I could (and still can), thanks to sampling bird cherry trees in Finland in the depths of winter, identify it in the dark by the smell of the bark 😊 In the mid-1980s, I jumped on to the species-area relationship bandwagon (Leather, 1985, 1986) and discovered the wonderful Biological Flora of the British Isles, hosted by the British Ecological Society. Armed with the arrogance of youth, and obviously at the time, not suffering from ‘imposter syndrome’, I contacted Arthur Willis (the then Editor of the series) and volunteered to write the entry for bird cherry. Pretty cheeky for an entomologist, but hey, both my parents were botanists and me and bird cherry were old pals! Arthur said yes and sent me the instructions for contributors which included all the headings and sub-sections required. It looked pretty straightforward to me; go down the headings, insert the information and write the narrative. Easy peasy lemon squeezy.  Or so I very naively thought ☹ I whipped through the headings, filled in the data that I had, wrote the accompanying narrative and posted it off to Arthur.  Job done! A few weeks later he returned my manuscript telling me that I was also expected to fill in the missing data gaps with data collected by me, not just leave them blank! 

Reality strikes!

So, over the next two years that is exactly what I did.  I checked out which mycorrhizae were associated with bird cherry, collected seed and calculated germination rates, sketched the different seedling stages, did NVC surveys at six different sites, characterised the growth structure of the tree and shrub forms and looked at responses to defoliation. I learnt a lot of botany! Arthur was an incredibly helpful editor and without his encouragement I would never have completed the entry.  I did, however, turn down Arthur’s suggestion that I do the entry for Prunus avium 😊

In 2018 I was contacted by Latha Menon, a Senior Commissioning Editor for OUP, who wanted to know if I would be interested in writing a book for their Very Short Introduction series, in this case, insects.  Having since 1990 grown older and picked up imposter syndrome on the way, I was initially a bit hesitant and asked if it would be possible to have a co-author.  Latha was somewhat lukewarm about this, saying that what the series was about was producing an extended essay (35 000 words) for a general audience reflecting the expertise and enthusiasm of the author.  I pondered about it and thought, well I’ve been a professional entomologist for more than forty years, and an amateur for my whole life, and taught entomology for more than thirty years, so how hard could it be to write 35 000 words about insects? I have also been blogging for what I have envisaged as a mixed audience since 2012, so surely within my capabilities?

I should have known better

It turns out that you can know too much about insects at the same time as you don’t know enough about them! First, I had to decide on a structure for the essay and also what particular aspects of entomology would leap off the page and grab my readers.  Much as I love aphids, other insects would have to feature.  The obvious place to start, I thought, would be to look at how our entomology course introduced the subject to new students, so Chapter 1, In the beginning was born. This was actually not that simple as I had to deal with the evolution of insects, their classification, their anatomy, a lot of their physiology, and also why they were and are so successful. Trying to make that not like a series of Wikipedia sections was not easy.

Now to me, one of the things that make insects so spectacular and evinces amazement in non-entomologists, is how good they are at reproducing themselves, hey presto, Chapter 2, Prolific procreators and the need to discuss sexual selection, mating behaviour, courtship, lekking and much more. I had originally planned to cover host selection and life history strategies in this chapter, but found that it didn’t sit very well in that context.

Instead, I moved on to Chapter 3, On the move, which began with the evolution of flight, much, of which, despite my decades of experience, was quite a revelation to me. From flight I moved onto host selection, and the physiology and ecology of specialist and generalist feeding. These first three chapters were the most difficult to write, bearing in mind that my readers need to understand the basics of how insects work to fully grasp the wonder of what insects are actually achieving. I had to rewrite these first chapters three times before my Commissioning Editor, my non-entomologist lay-reader (my wife, a humanities graduate), a botanist colleague and an entomological colleague, were happy with them.

Those chapters behind me, I now felt it was time to move on to those aspects of entomology that had super wow factor, those facts that would make my readers exclaim things like “I didn’t know that” and encourage them to pass them on to their friends and relatives. Heavily influenced by my childhood love of social insects, Chapter 4, Living together, appeared on the scene. As well as talking about the well-known bees, ants and termites, it also gave me the chance to discuss lesser known examples such as dung beetles, social bugs, insect symbionts, insect-plant interactions, and yes, of course, aphids get more than a passing mention😊

The next three chapters are a bit niche, but gave me the chance to launch Chapter 5, Aquatic Insects, into the mix and talk about the importance of freshwater insects and even more excitingly, wax lyrical about the little known truly marine Ocean Skaters, which I first came across on a work trip to Mauritius in the mid-1990s. Judging by what I see on social media platforms, non-entomologists are, in the English vernacular, totally gob-smacked by how insects can pretend to be something else, so this made Chapter 6, Crypsis, mimicry and blatant advertising, an obvious heading.  I had a lot of fun with this, but was slightly hampered by the restriction placed by OUP on how many illustrations I was allowed to include, and also sadly not being allowed colour.

To me, the ability of insects to live in very inhospitable conditions, from deserts, to ice caves, to mountain tops and to survive arctic winters and other extreme weather conditions without the benefit of fur coats and cold baths, made Chapter 7, Against the odds, a natural.

I have, over the years, been amazed by how limited many people’s appreciation of the positive economic, social, artistic and health benefits of insects to the human world are (Leather, 2015), hence Chapter 8, The good, the bad and the ugly.  Here I dealt with pests, disease vectors, biological control, maggot therapy, pollinators, the role of insects as ecosystem engineers, as waste-disposal specialists and as recyclers.

I began my book by describing the diversity and ubiquity of insects. I discussed their origins and marveled at the ways in which insects have adapted to a wide range of environments and the roles that they play in maintaining ecosystem health. Given that for at least the last twenty years or so, entomologists and ecologists have been warning about the dangers of losing species I felt it fitting to end it by discussing the harm that we are doing to insects and the planet that we, and they, inhabit, and ways in which we might act to halt or reverse our course, if it is not already too late.  I finished with a warning, and the hope that we are not too late to stem disaster, Chapter 9, Ecological Armageddon—insects in decline?

It was, primarily due to the fact that at times, for every word I took out, I seemed to add another ten, both one of the most frustrating but also satisfying pieces of writing that I have ever done. I just hope that when it hits the shops, my readers will find as much to enjoy as I have since I first came across insects just over sixty years ago.

References

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. (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 hostrange, plant architecture, age of establishment, taxonomic isolation and species-area relationships. Journal of Animal Ecology, 55, 841-860.

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

Leather, S.R. (2015) Influential entomology: a short review of the scientific, societal, economic and educational services provided by entomology. Ecological Entomology, 40 (Suppl. 1), 36-44.

Leather, S.R. & Bland, K.P. (1999) Insects on Cherry Trees, Richmond Publishing Co, Ltd, Slough.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Local – (101-300 UK hectad records)

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

References

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

Bell, J.R., Alderson, L., Izera, D., Kruger, T., Parker, S., Pickup, J., Shortall, C.R., Taylor, M.S., Verier, P. & Harrington, R. (2015) Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. Journal of Animal Ecology, 84, 21-34.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

*It never ceases to amaze me how many keen gardeners are determined to weed out all the native nectar bearing plants (wees) in their gardens and replace them with useless, gaudy, domesticated, infertile and non-native prima donnas and green deserts!

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

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

 

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.

 

Satiable curiosity – side projects are they worthwhile?

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

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

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

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

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

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

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

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

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

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

 

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

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

 

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

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

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

 

Side project 5. Sixty bird cherry trees 1993-2012

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

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

 

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

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

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

 

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

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

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

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

 

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

*

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

**

My second post-doc was only for two years.

***

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

 

Not all aphid galls are the same

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

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

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

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

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

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

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

The grand plan!

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

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

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

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

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

The Sixty Tree site April 2006.

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

 

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

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

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

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

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

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

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

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

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

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

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

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

Number of Prunus padus trees with severe deer damage

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

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

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

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

References

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

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

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

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

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

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

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

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

 

 

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

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

Ideas I had and never followed up

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

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

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

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

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

The Forgotten Nine

 

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

In those days we used graph paper 🙂

 the data, do let me know.

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

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

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

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

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

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

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

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

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

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

 

References

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

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

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

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

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

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

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

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

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

 

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

**Now Vice-Chancellor of the University of Wollongong

 

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

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

Red, green and gold, all on one tree

When Frank Sinatra sang Autumn Leaves he was almost certainly not thinking of aphids and I am pretty certain that the English lyricist, Johnny Mercer, who translated the words from the original French by Jacques Prévert wasn’t either 🙂

The colours we see in autumn are mainly due to two classes of pigment, the carotenoids (yellow-orange; think carrot) and the anthocyanins (red-purple).  Carotenoids are present in the leaves all year round but are masked by the green chlorophyll.  Chlorophyll breaks down in autumn, leaving the yellow carotenes visible.  The anthocyanins on the other hand are not formed until autumn (Sanger, 1971; Lee & Gould, 2002) and this mixture of pigments give us the colours that have inspired so many artists.

Autumn Leaves Georgia O’Keeffe (1924) Tate Modern

To many, autumn starts with the appearance of the first turning leaves, to me it is the arrival of gynoparae* of the bird cherry-oat aphid (Rhopalosiphum padi) on my bird cherry (Prunus padus) trees.

Bird cherry, Prunus padus, leaves on the turn.

Little did I know when I started my PhD in 1977 that almost thirty years later I would be part of a raging debate about the function of autumn colouration in woody plants. At the time I was interested in the colonisation patterns (or as I pretentiously termed it in my thesis ‘remigration’) of bird cherry aphids from their secondary grass and cereal host plants to their primary host bird cherry.  My study system was 30 bird cherry saplings divided between two cold frames in the Biology Compound at the University of East Anglia (Norwich).  Every day from the middle of August until leaf fall I checked every leaf of each tree, for gynoparae, males and oviparae, carefully noting the position of each leaf, its phenological stage and giving it a unique number. I repeated this in the autumns of 1978 and 1979.  The phenological stage was based on the leaf colour: green, mature; yellow, mature to senescent; red, senescent.  What I reported was that more gynoparae landed on green and yellow leaves than on red and that the gynoparae on green and yellow leaves survived for longer and produced more offspring (oviparae), than those on red leaves (Leather, 1981).   The gynoparae of the bird cherry aphid are quite special in that although as adults they do not feed (Leather, 1982), they do not land on bird cherry trees at random (Leather & Lehti, 1982), but choose trees that not only do their offspring (the oviparae) do better on, but that also favour those aphids hatching from eggs in the spring (Leather, 1986).  It should not have come as a surprise then, that when I analysed some of the data I had collected all those years ago, their preference for green and yellow leaves over red ones, is linked to how long those

Figure 1. Length of time leaves remained on tree after first colonisation by gynoparae of Rhopalosiphum padi (F = 30.1 df 2/77, P <0.001)

leaves have left to live (Figure 1). The timing of events at this time of year, has, of necessity, got to be very precise. The egg-laying females (oviparae) are unable to develop on mature bird cherry leaves (Leather & Dixon, 1981), but it seems that the bird cherry aphid has this under control, making its decisions about the timing of the production of autumn forms (morphs) sometime in August (Ward et al., 1984).  All very sensible as far as I was concerned and that was as far as I took things.  Subsequent work by Furuta (1986) supported this in that he showed that maple aphids settled on and reproduced on green-yellow and yellow-orange leaves but avoided red leaves which had shorter life spans.

Jump forward fifteen years or so, and in a paper, that at the time, had somehow passed me by, the late great Bill Hamilton and Sam Brown (Hamilton & Brown, 2001) hypothesised that trees with an intense autumn display, similarly to those brightly coloured animals that signal their distastefulness with yellows, blacks and reds, were signalling their unsuitability as a host plant to aphids.  Like the costs imposed on insects that sequester plant toxins to protect themselves against predators, the production of anthocyanins responsible for the red autumn colouration is expensive, especially when you consider that the leaves have only a short time left to live (Hoch et al., 2001).  In autumn, trees and woody shrubs are normally mobilising resources in the leaves and moving them back into themselves ready to be used again the following spring (Dixon, 1963). Ecologists and evolutionary biologists were thus keen to explain the phenomenon in terms of trade-offs, for example, fruit flags that advertise the position of fruits for those trees that rely on seed dispersal by vertebrates (Stiles, 1982) or as ultra-violet screens to prevent tissue damage (Merzlyak & Gittelson, 1995).  Hamilton & Brown felt that these hypotheses were either, in the case of the fruit flag, only applicable to trees with fruit present and, in the latter, untenable. Instead they advocated the ‘signalling hypothesis’ which was based on the premise that trees that suffer from a lot of aphids (attacked by more than one species rather than by large numbers of a single species), invest in greater levels of defence and in autumn advertise this using bright warning colours.   The premise being, that although it is metabolically expensive for the plants to produce these colours, it is worth the investment if they result in a reduction in aphid attack.

This hypothesis was not without its detractors. Others suggested, that far from avoiding red colours, aphids were attracted to yellow or green as an indicator of host nutrition (Wilkinson et al., (2002).  Holopainen & Peltonen (2002) also suggested that birch aphids use the onset of autumn colours to pick out those trees where nutrient retranslocation was happening, and thus with higher levels of soluble nitrogen in the leaves.  This was of course, what I was trying to confirm back when I was doing my PhD.  Conversely, supporters of the signalling hypothesis, argued that trees (birch again) that could ‘afford’ to produce bright autumn colours were fitter, so more resistant in general and that they were warning potential herbivores of this by a bright autumn display (Hagen et al 2004).

Round about this time (2002), I was approached by a young Swiss researcher, Marco Archetti, who knew that I had a plot of sixty bird cherry trees that I had planted up when I arrived at Silwood in 1992, originally designed to follow-up some work that I had begun whilst at the Forestry Commission looking at the effects of early season defoliation on subsequent tree growth (Leather, 1993, 1995).  Marco convinced me that I had the ideal set-up to test the ‘signalling hypothesis’ and what was to be a very fruitful collaboration began.

We counted arriving gynoparae and their offspring (oviparae) throughout October (Marco making trips over from Oxford where he was then based**) noting leaf colour before and after each count.  As with my PhD work we found that the greener trees were preferentially colonised by the gynoparae and that more oviparae were produced on those trees and that given what I had found earlier that bird cherry aphid gynoparae chose trees that are good hosts in spring (Leather, 1986), Marco felt that we were able to support the honest signalling hypothesis (Archetti & Leather, 2005).  I was slightly less comfortable about this, as there are only two species of aphid that attack bird cherry and one of those is very rare and the original signalling hypothesis was based on the premise that it was trees that were attacked by a lot of aphid species that used the red colouration as a keep clear signal.  Anyway, it was published 🙂

That said, others agreed with us, for example, Schaefer & Rolshausen (2006) who called it the defence indication hypothesis, arguing that bright colours advertise high levels of plant defence and that the herbivores would do well to stay away from those plants displaying them. On the other hand, Sinkkonen (2006) suggested that reproductively active plants produce autumn colours early to deter insects from feeding on them and thus reduce their seed set.

Chittka & Döring (2007) on the other hand, suggested that there is no need to look further than yellow carotenoids acting as integral components of photosynthesis and protection against light damage and red anthocyanins preventing photo-inhibition (Hoch et al., 2001) as to why trees turn colourful in autumn.  In other words, nothing to do with the insects at all.  A couple of years later however, Thomas Döring and Marco got together with another former colleague of mine from Silwood Park, Jim Hardie, and changed their minds slightly.  This time, whilst conceding that red leaves are not attractive to aphids but noting that yellow leaves are even more attractive than green ones, suggested that the red colour could be being used to mask yellow (Döring et al., 2009).

Others have their own pet theories.  In recent years, veteran Australian entomologist Tom White has become interested in the concept of insect species that specifically feed on senescent plant tissue (White, 2002, 2015) and added to the debate by suggesting that aphids in general are senescence feeders and thus choose green and yellow as they have longest time to live and that the red leaves are also nitrogen depleted (White, 2009) which is supported by my PhD data (Figure 1).  This resulted in a spirited response by Lev-Yadun & Holopainen (2011) who claimed that he had misunderstood the scenario in thinking that leaves go sequentially from green to yellow to red, which they suggest is rare (I question this) and that actually in trees that go from green to red, the leaves still contain significant amounts of nitrogen, so a deterrent signal is still required.

Maple, green to yellow in this case

Spindle, Euonymus europaeus, green to red

What about those trees and other plants that have red or purple leaves in the spring or all year round and not just in autumn?

Some trees have red foliage all year

Trees like some of the ornamental cherries or copper beech? I haven’t been able to find any papers that suggest that red or purple-leaved varieties of beech and cherries are less susceptible to aphid attack.  My own observations, probably imperfectly recalled, are that copper beech is regularly infested by the beech woolly aphid, Phyllaphis fagi , and just as heavily, if not more so than the normal green-leaved  beech trees.  That of course may just be a reflection that the white waxy wool covering the aphid stands out more against the red leaves.  Perhaps someone out here might like to check this out?  Some work that my friend and former colleague, Allan Watt, (sadly unpublished) did many years ago in Scotland looking at the effect of beech species and cultivar on infestation levels by the beech leaf mining weevil, Rhynchaenus fagi, did not indicate any differences between copper and green cultivars.  It does seem however, that in cabbages, leaf colour can tell the specialist cabbage aphid, Brevicoryne brassciae, if plants are well defended or not, the bluer the cabbage, the nastier it is (Green et al, 2015).

To summarise:

1. Red leaves are produced by the trees in autumn to reduce ultraviolet damage and protect metabolic processes in the leaf.
2. Red leaves are deliberately produced by the tree to warn aphids that their leaves are well defended – honest signalling.
3. Red leaves are produced by the tree to ‘fool’ the herbivores that the leaves are likely to drop soon and warn them to keep away so as to safeguard their fruit – dishonest signalling.
4. The tree is blissfully unaware of the aphids and the aphids are exploiting the intensity of the autumn colours produced by the trees to select which are the best trees to colonise in terms of nutrition and length of time left on the tree.

As I write, the debate still goes on and we seem no nearer to arriving at a definitive answer to the riddle of why trees produce bright leaves in autumn.  If nothing else however, the debate has generated a lot of interest and enabled people to sneak some amusing titles into the scientific literature.  Do make the effort to read the titles of some of the references below.

References

Archetti, M. (2009) Phylogenetic analysis reveals a scattered distribution of autumn colours. Annals of Botany, 103, 703-713.

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

Chittka, L. & Döring, T.F. (2007) Are autumn foliage colors red signals to aphids? PLoS Biology , 5(8): e187. Doi:10.1371/journal.pbio.0050187.

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Döring, T.F., Archetti, M. & Hardie, J. (2009) Autumn leaves seen through herbivore eyes.  Proceedings of the Royal Society London B., 276, 121-127.

Furuta, K. (1986) Host preferences and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera: Aphididae). Zeitschrift fur Angewandte Entomologie, 102, 93-100.

Green, J.P., Foster, R., Wilkins, L., Osorio, D. & Hartley, S.E. (2015) Leaf colour as a signal of chemical defence to insect herbivores in wild cabbage (Brassica oleracea).  PLoS ONE, 10(9): e0136884.doi:10.1371/journal.pone.0136884.

Hagen, S.B. (2004) Autumn coloration as a signal of tree condition. Proceedings of the Royal Society London B, 271, S184-S185.

Hamilton, W.D. & Brown, S.P. (2001) Autumn tree colours as handicap signal. Proceedings of the Royal Society London B, 268, 1489-1493.

Hoch , W.A.,  Zeldin, E.L. & McCown, B.H. (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology, 21, 1-8.

Holopainen, J.K. & Peltonen, P. (2002) Bright colours of deciduous trees attract aphids: nutrient retranslocation hypothesis.  Oikos, 99, 184-188.

Leather, S.R. (1981) Reproduction and survival: a field study of the gynoparae of the bird cherry-oat aphid, Rhopalosiphum padi (L.). Annales Entomologici Fennici, 47, 131-135.

Leather, S.R. (1982) Do gynoparae and males need to feed? An attempt to allocate resources in the bird cherry-oat aphid Rhopalosiphum padi.  Entomologia experimentalis et applicata, 31, 386-390.

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

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

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

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

Leather, S.R. & Lehti, J.P. (1982) Field studies on the factors affecting the population dynamics of the bird cherry-oat aphid, Rhopalosiphum padi (L.) in Finland. Annales Agriculturae Fenniae, 21, 20-31.

Lee, D.W. & Gould, K.S. (2002) Anthocyanins in leaves and other vegetative organs: An introduction. Advances in Botanical Research, 37, 1-16.

Lev-Yadun, S. & Holopainen, J.K. (2011) How red is the red autumn leaf herring and did it lose its red color? Plant Signalling & Behavior, 6, 1879-1880.

Merzlyak, W.N. & Gittelson, A. (1995) Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescing leaves (Acer platanoides L.). Journal of Plant Physiology, 145, 315-320.

Sanger, J.E. (1971) Quantitative investigations of leaf pigments from their Inception in buds through autumn coloration to decomposition in falling leaves.  Ecology, 52, 1075-1089.

Schaefer, H.M. & Rolshausen, G. (2006) Plants on red alert – do insects pay attention?  BioEssays, 28, 65-71.

Sinkkonen, A. (2006) Do autumn leaf colours serve as reproductive insurance against sucking herbivores?  Oikos, 113, 557-562.

Stiles, E.W. (1982) Fruit flags: two hypotheses. American Naturalist, 120, 500-509.

Ward, S.A., Leather, S.R., & Dixon, A.F.G. (1984) Temperature prediction and the timing of sex in aphids. Oecologia, 62, 230-233.

White, T.C.R. (2003) Nutrient translocation hypothesis: a subsect of the flush-feeding/senescence-feeding hypothesis. Oikos, 103, 217.

White, T.C.R. (2009) Catching a red herring: autumn colours and aphids. Oikos, 118, 1610-1612.

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

Wilkinson, D.M., Sherratt, T.N., Phillip, D.M., Wratten, S.D., Dixon, A.F.G. & Young, A.J. (2002) The adaptive significance of autumn colours.  Oikos, 99, 402-407.

 

 *for a detailed account of the wonderful terminology associated with aphid life cycles read here

**coincidentally he is now a Lecturer at the University of East Anglia in the same Department where I did my PhD

Mellow Yellow – Not all aphids live on green leaves

I have written before about aphids and how their quest for the ideal food plant may explain the evolution of host alternation; we find that most aphid species tend to be associated with rapidly growing meristems, or newly flushing leaves (Dixon, 2005). Some aphids are so keen on young plant tissue that they ‘engineer’ youth in their host plants, injecting salivary compounds and forming leaf–rolls, pseudo-galls and galls, all of which act as nutrient sinks and lengthen the time that the modified leaves stay green and nutrient-rich

 Leaf-roll caused by Rhopalosiphum padi on bird cherry, Prunus padus.

Pronounced leaf roll pseudo-gall caused by Myzus cerasi on Prunus avium.

Non host-alternating (autoecious) aphids, such as the sycamore aphid Drepanosiphum platanoidis, the maple aphid, Periphyllus testudinaceus, or the birch aphid, Euceraphis punctipennis, have no such escape route; they are confined to their tree host for the year, albeit, they can, if they ‘wish’, fly to another tree of the same species, but essentially they are held hostage by the their host plant. As the season progresses, leaf nutritional and physical properties change; going from young tender green leaves, with high nitrogen and water contents, to mature, tough leaves, low in nitrogen and water to yellow senescing leaves with again, higher nitrogen levels (Awmack & Leather, 2002) and finally of course, dead brown leaves of no nutritional value.

Sycamore and maple aphids, enter a state of suspended animation ‘summer aestivation’ (Essig, 1952; Dixon, 1963), whilst birch and poplar aphids, whose hosts plants often produce new growth during the year, ‘track’ these new leaves (Wratten, 1974; Gould et al., 2007). As far as these aphids are concerned young tissue is their best food source, with senescent tissue being second best and mature leaves being least favoured. During the summer they will, however, take advantage of mature leaves that are prematurely senescing, such as those attacked by leaf diseases such as tar spot. I have often found sycamore aphids feeding and reproducing on these infected leaves whilst those aphids on neighbouring mature leaves remain in aestivation.

Effects of tar spot on sycamore leaves

Host-alternating (heteroecious) aphids on the other hand are somewhat different. As their life cycle includes a programmed migration back to their primary tree host in autumn, those autumn morphs (oviparae) are adapted to senescent tissue (Leather & Dixon, 1982, Kundu & Dixon, 1993, 1994). Similarly, the spring morphs (fundatrices and fundatrigeniae) are adapted to young leaves and find it difficult or impossible, to make a living on senescent leaves.

There are yet other aphids, such as the green spruce aphid Elatobium abietinum, the pine aphid, Eulachnus agilis and the black pecan aphid, Melanocallis caryaefoliae, that are senescence specialists. In contrast to the flush specialists, these aphids engineer senescence, also using salivary compounds,  and are unable to survive on young foliage (Bliss, 1973; Fisher, 1987; Cottrell et al., 2009).

Elatobium abietinum ‘engineering’ senescence on spruce needles and avoiding young flushing tissue.

It is interesting to speculate that perhaps these tree-dwelling non host-alternating aphids are secondarily derived from the autumn part of the life-cycle of host-alternating aphids. After all, if non host-alternating aphids on herbaceous host plants are off-shoots of the summer part of the host-alternating life-cycle why not the other way round. There is just so much more to learn about aphids. Yet another reason why I love aphids so much 😉

References

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

Bliss, M., Yendol, W.G., & Kearby, W.H. (1973) Probing behaviour of Eulachnus agilis and injury to Scotch pine. Journal of Economic Entomology, 66, 651-655.

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

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Dixon, A.F.G. (2005) Insect Herbivore-Host Dynamics. Cambridge University Press, Cambridge.

Fisher, M. (1987) The effect of previously infested spruce needles on the growth of the green spruce aphid, Elatobium abietinum. Annals of Applied Biology, 111, 33-41.

Gould, G.G., Jones, C.G., Rifleman, P., Perez, A., & Coelman, J.S. (2007) Variation in Eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behaviour of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae). Environmental Entomology, 36, 1212-1225.

Kundu, R. & Dixon, A.F.G. (1993) Do host alternating aphids know which plant they are on? Ecological Entomology, 18, 61-66.

Kundu, R. & Dixon, A.F.G. (1994) Feeding on their primary host by return migrants of the host alternating aphid, Cavariella aegopodii. Ecological Entomology, 19, 83-86.

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

Wratten, S.D. (1974) Aggregation in the birch aphid, Euceraphis punctipennis (Zett.) in relation to food quality. Journal of Animal Ecology, 43, 191-198.

 

Post script

A lot of what I describe comes from a talk I gave in 2009 at a workshop in Oxford on autumn colours (the output of which was Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., & Thomas, H. (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology & Evolution, 24, 166-173. I always meant to write the talk up as an Opinion piece but procrastination set in badly. I was somewhat annoyed with myself when earlier this year this excellent piece by the legendary ecologist and entomologist, Tom White, appeared; I have only myself to blame, six years is a very long bit of procrastination 😉

White, T.C.R. (2015) Senescence-feeders: a new trophic sub-guild of insect herbivores Journal of Applied Entomology, 139, 11-22.

 

Post post script

This post is dedicated to my eldest son, Sam, who died quietly in his sleep, at a tragically young age, December 23^rd 2010.   It would have been his birthday on the 21st May.  Despite being a molecular biologist, (he worked at the Sanger Institute), he was as green as you can get, a great naturalist and conservationist, with an incredibly gentle soul. He strongly believed in conserving the World’s natural resources and amused colleagues by sticking up signs in the toilets at the Sanger, which read “If its yellow let it mellow, if its brown flush it down”.

 

He is sorely missed by us all. He also had more Nature papers than me 😉

Parkhill, J., Achtman, M., James, K.D. et al., (2000) Complete DNA sequence of a serogroup A strain of Neisseria meningitides. Nature, 404, 502-506

Parkhill, J., Dougan, G. , James, K.D. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature, 413, 848-852.

Parkhill, J., Wren, B.W., Thomson, N.R. et al., (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523-527.

Parkhill, J., Sebaihia, M., Preston, A. et al., (2003) Comparative analysis of the genome sequences of Bordetella pertussis,   Bordetella parapertussis and Bordetella bronchiseptica. Nature Genetics, 35, 32-40

Wood, V., Gwilliam, R. Rajandream, M.A. et al., (2002) The genome sequence of Schizosaccharomyces pombe . Nature, 415, 871-880

 

 

Not all Aphids are Pests

Unfortunately when you mention the word aphid most people’s first thought is PEST!  It is true that they are perhaps the most important insect pests of crops

            

in temperate regions of the world, and that in the UK they are serious pests of cereals, sugar beet, beans, vegetables and glasshouse crops.  It has been estimated that crop losses due to feeding damage and/or virus transmission exceed £100 million per annum http://www.scri.ac.uk/research/pp/pestanddisease/insectmiteecology/virusvectorinteractions .  On the other hand this is down to only about 250 species which out of a total of 5000 described species is not very many (about 5%).  Not only are most aphids playing useful roles in ecosystems acting as food sources to other insects, arthropods and dare I say it, vertebrates 😉 . They also play an important part in the decomposition cycle (Choudhury, 1985).  The thing that most people don’t realise is that some aphids are incredibly rare. Some are rare because of their close associations with rare plants, others rare because of a complex relationship with ants https://simonleather.wordpress.com/2013/12/05/not-all-aphids-live-on-leaves/ and some for no apparent reason at all.  For example, there are two aphid species that live on bird cherry (Prunus padus),  Rhopalosiphum padi, an extremely common aphid, host-alternating between bird cherry and grasses, and a major pest of cereals in temperate countries (Leather et al., 1989) and Myzus padellus, host-alternating between bird cherry and members of the Labiatae (Galeopsis spp. (Hemp nettle)) and Scrophulariaceae (Pedicularis spp. and Rhinanthus sp., members of the snapdragon family).  In all my many years of sampling bird cherry I have never seen Myzus padellus, yet their life-cycles and habits are strikingly similar, so why is the latter so rare?  No one knows.

Similarly, on birch we find, not very often because it is so rare, Monaphis antennata , which unlike most aphids, lives as a nymph (immature) on the upper side of birch leaves, possibly

to escape natural enemies as the much more common species of birch aphids, Euceraphis punctipennis and Betulaphis quadrituberculata like the majority of leaf-feeding aphids, both live on the underside of leaves, which is where aphid predators normally forage (Hopkins & Dixon 1997). I have seen this aphid once, shown to me by the late Nigel Barlow http://newzealandecology.org/nzje/free_issues/NZJEcol30_1_1.pdf  when he visited me at Silwood Park in the late 1990s.  Despite repeated visits to the same trees that we found Monaphis on, I have never seen it again.  So far no one has been able to explain why it is so rare (Hopkins et al., 1998).  Interestingly enough, apart from keys and identification manuals, it has rarely been written about; Web of Knowledge reveals only four research papers on it.

There are many more rare aphids hiding out there, a number of which have only ever been seen by the entomologist who first described them and no doubt even more who have not yet been found, as is the cases with many more insect species  – not enough insect taxonomists, not enough funding.

Choudhury, D. (1985) Aphid honeydew – a re-appraisal of Owen and Wiegert’s hypothesis. Oikos, 45, 287-289. http://www.jstor.org/discover/10.2307/3565718?uid=3738032&uid=2&uid=4&sid=21103382740253

Hille Ris Lambers, D. & Rogerson, J.P. (1946) A new British aphid from Prunus padus L.  Myzus padellus sp n. (Hemiptera, Aphididae). Proceedings of the Royal Entomological Society of London, 15, 101-105 http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3113.1946.tb00833.x/abstract

Hopkins, G.W. & Dixon, A.F.G. (1997) Enemy-free space and the feeding niche of an aphid. Ecological Entomology, 22, 271-274. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2311.1997.00075.x/full

Hopkins, G.W. & Dixon, A.F.G. (2000)  Feeding site location in birch aphids (Sternorrhyncha: Aphididae): the simplicity and reliability of cues.  European Journal of Entomology, 97, 279-280 http://www.eje.cz/pdfs/eje/2000/02/19.pdf

Hopkins, G.W., Thacker, J.I., & Dixon, A.F.G. (1998) Limit to the abundance of rare species: an experimental test with a tree aphid. Ecological Entomology, 23, 386-390. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2311.1998.00163.x/full

Leather, S.R., Walters, K.F.A., & Dixon, A.F.G. (1989) Factors determing 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. http://journals.cambridge.org/download.php?file=%2FBER%2FBER79_03%2FS0007485300018344a.pdf&code=8d6d2144666846ebb5d589f01343f27c