Tag Archives: sycamore

Data I’m never going to publish – factors affecting sycamore flowering and fruiting patterns

As a teenager I used to have a favourite thinking place, underneath a large beech tree half-way down the school drive.  I used to watch the activities of my school mates, while contemplatively chewing beech nuts (my school friends found this mildly disgusting).

Some years beech nuts were much easier to find than others; although I didn’t realise it at the time, this was my introduction to the phenomenon of masting.  At this point I had better fill you in on the basics of tree reproduction. Like most plants, trees reproduce by producing flowers that are pollinated, depending on the species, by vertebrates, insects or the wind. The fertilised flowers then produce seeds that are housed in what we term fruit or cones, and which in many cases aid their dispersal. Reproduction is energetically a costly process, reserves channelled to reproduction cannot be use for growth and defence.  Trees have evolved three different approaches to this problem. Some trees produce a moderate number of seeds in most years, others have an Irregular fruiting pattern and some, such as beech and oak, have strongly periodic fruiting patterns, “mast” years.  Interestingly (my wife hates me starting sentences off like this), trees that mast are wind pollinated.

Beech (Fagus sylvatica) mast production over a sixteen year period in England. Data from Hilton & Packham (1997

You might wonder why, if reproduction is costly, that some trees are ‘willing’ to expend so much energy in one go.  There are two schools of thought regarding this. One, which I find fairly convincing, is the “predator satiation” hypothesis (Janzen, 1971).  This basically says that the trees, by having on and off years, starve their specialist seed predators in the off years, thus reducing predator pressure by killing lots of them off. In the mast years, there are enough seeds to feed the surviving predators and produce another crop of trees.  A more recent, and less exciting suggestion (to me anyway), is that if the trees have a mass synchronised flowering effort, i.e. a mast year, then the chances of being pollinated are greatly increased (Moreira et al., 2014).

People tend to associate masting with trees that produce heavy fruit, acorns, hazel nuts and beech nuts for example, and I was no exception, so it wasn’t until a couple of years (1995) after I started my mega-sycamore study at Silwood Park that I had a bit of a revelation. I realised that not all of the trees flowered and that there seemed to be a lot fewer seeds that year than I remembered there being the year before. Sycamore seeds come equipped with two little wings (they are wing dispersed) and occur in little bunches (infructescences) so are quite noticeable.

Winged sycamore seed and ‘bunch’ of sycamore fruit

My sycamore study was one of my many side projects set up to satisfy my’ satiable curiosity’ and I had, at the time thought that I had made sure I was measuring everything that could possibly interact with the aphids feeding on the trees. I had, however, somehow overlooked sycamore flower production 🙂 I had taken into account that in some years the sycamore aphid can be present in huge numbers and and I was well aware from the work of my PhD supervisor

Sycamore aphids emerging in spring – some years you can see even more on the newly flushing buds

Tony Dixon, that the aphids can cause substantial losses to tree growth (Dixon, 1971), so had included tree girth and height measurements into my massive data collection list. Strangely, however, despite knowing from my work with

The effect of the sycamore aphid, Drepanosiphum platanoidis, on leaf area of two sycamore, Acer pseudoplatanus, trees over an eight year period (Dixon 1971).

the bird cherry-oat aphid Rhopalosiphum padi, that even quite low numbers of aphids could have substantial negative effects on cherry production (Leather, 1988), I had totally overlooked sycamore flowering and seed production. I am just thankful, that I only missed three years of flowering data 🙂

The effects of bird cherry aphid infestation on reproductive success of the bird cherry, Prunus padus (Leather, 1988)

Unlike the rest of my sycamore data set, the flowering data collection was actually set up to test a hypothesis; i.e. that aphid numbers affected flowering and seed set. Sycamore is in some ways similar to the well-known masting species such as oak and beech in that it is (jargon coming up) heterodichogamous. All flowers are functionally unisexual and appear sequentially on a single inflorescence. The inflorescences can however be either protandrous, i.e. male anthesis takes place before the stigmas become receptive, or protogynous where the reverse sequence takes place. Where it differs from the typical masting species is that is produces wind dispersed seeds and is wind and insect pollinated; oak, beech and hazel are entirely wind pollinated.  Pierre Binggelli, then based at the Unibersity of Ulster, hypothesised that protandrous trees may suffer less herbivore damage than protogynous trees (Binggeli, 1992). He suggested that protogynous trees, having less energy available to invest in defensive chemistry, are more attractive to insect herbivores, particularly chewers. On the other hand, sycamore trees that have been subject to previous insect infestation have fewer resources available to produce female flowers, become protandrous and avoid infestation by herbivores the following year. Presumably the next year, having escaped insect attack by being protandrous they should become protogynous again. So, if I wanted to test this hypothesis, I needed to learn how to sex sycamore flowers. Despite a handy guide that I came across (Binggeli, 1990), ) I found it almost impossible, to do, so

A. Protogynous inflorescence (female II flowers of Mode G are male II in Mode B). B. Protogynous infructescence, Mode B. C. Protogynous infructescence, Mode G. D. Protandrous inflorescence.
E. Protandrous infructescence. F. Vegetative shoot, G. Flowering shoot (Mode E).
H. Fruiting shoot (Flowering Modes B,C,D & G). (From Binggeli, 1990)

contacted Pierre, who very kindly agreed to check some of my ‘guesses’ for me.  Despite this help, I still found it very difficult so opted (very unwisely as it turned out) to collect fruit samples from each tree, put them in paper bags, and bring them back to the lab for sexing at a later date.  As you have probably guessed, I ended up with lots of paper bags which I then, not very cleverly, stored in plastic bin bags.  This went on for several years as I kept putting off the day when I would have to sit down and sex several thousand bunches of sycamore fruit. Then came the happy disastrous day when I came back from holiday to find out that the cleaners had disposed of my bin bags. To tell the truth I was not that upset as it gave me an excuse to stop collecting the fruit samples and reduced my feelings of guilt about having huge piles of unsexed sycamore fruit bunches cluttering up the lab 🙂 I did, of course, carry on counting the number of flowers on the trees, which was much easier data to collect and analyse.

I reluctantly ended my study in 2012 when I left Silwood Park for pastures new, but despite this I still haven’t analysed all my sycamore data, although I was very happy a couple of years ago when a PhD student from the University of Sheffield (Vicki Senior) volunteered to analyse some of my sycamore aphid data which was published last year (Senior et al., 2020). The winter moth data and orange ladybird data are also being analysed by a couple of my former students and hopefully will also be published by next year.

So what does the sycamore fruiting data show? Well, first, despite sycamore being reproductively somewhat atypical of other masting trees species, I would contend that my 17-year data set of sycamore fruit production looks remarkably similar to the Hilton and Packham beech masting data set. I am thus confident in stating that sycamore is a masting species.

Mean sycamore fruit production at Silwood Park, averaged from 52 trees 1996-2012,

Am I able to link sycamore seed production with aphid abundance, is the fruiting pattern a result of herbivory?  I can’t test Pierre Binggeli’s hypothesis about sex changing trees, because I lost the data, but I can try and see if aphid infestation affects fruit production. The two most common aphid species on the Silwood Park sycamore trees are the sycamore aphid Drepanosphum platanoidis and the maple aphid, Periphyllus acericola.  

Mean sycamore aphid and mean maple aphid loads (average annual counts per 40 leaves from all trees) 1996-2012.

They can both occur in high numbers, but in general, the average numbers of P. acericola are much higher than D. platanoidis. The reason why P. acericola has much higher numbers is a result of its over-summering strategy.

Over-summering morphs of the sycamore and maple aphid. Images from https://influentialpoints.com/Gallery/Drepanosiphum_platanoidis_common_sycamore_aphids.htmhttps://influentialpoints.com/Gallery/Periphyllus_acericola_Sycamore_Periphyllus_Aphid.htm#other

While the sycamore aphid spends the summer aestivating (basically a summer version of hibernation in that metabolism is reduced and reproduction ceases), the maple aphid produces a huge number of nymphs, known as dimorphs, which over-summer in dense, immobile aestivating colonies.  The sycamore aphid can escape predators by flying off the leaves if disturbed, the maple aphid dimorphs on the other hand, rely on their huge numbers to ensure survival of some of them over the summer to resume development and reproduce as autumn approaches, a form of predator satiation. They thus suffer a huge reduction in numbers compared with the sycamore aphid. (I must publish that one day). This makes drawing conclusions about the of herbivory (aphid feeding) on the trees a bit difficult.

Mean combined aphid load, showing how the number of dimorphs of the maple aphid skew the perceived aphid load.

Given that Tony Dixon showed that sycamore aphids cause a significant reduction in tree growth (Dixon, 1971), I

Relationship between mean combined aphid load (sycamore and maple aphid) and mean sycamore fruit production.

expected to see a negative relationship between aphid numbers and fruit production. What I did find was that there was a significant positive relationship between sycamore aphid numbers and fruit production, i.e. the more sycamore aphids, the more fruit produced, whereas with the maple aphid it was the other way round, more maple aphids, fewer fruit. If I combined the aphid loads, then the relationship becomes significantly positive, the more aphids you get the


Relationship between mean combined aphid load and the number of sycamore fruit produced the following year.

significantly negative relationship between aphid numbers and sycamore fruit production, but as I pointed out earlier this is driven by the preponderance of maple aphid dimorphs in the summer. You might also argue, that rather than looking at aphid numbers and sycamore fruit production in the same year, I should be comparing aphid numbers with fruit production the following year, i.e. a lag effect. I did indeed think of this, and found that there was, for both aphid species, no significant relationship between aphid numbers the previous year and fruit produced the following year. In fact, if I was an undergraduate student I would point out that there was a positive trend between aphid numbers and fruit production 🙂  If I do the same analysis using the combined aphid load, then the relationship becomes significantly positive, the more aphids you get the more sycamore fruit you get the following year which although counter-intuitive fits with the idea that stressed trees tend to produce more offspring (seeds) (Burt & Bell, 1991) and given that we know from Tony Dixon that the sycamore aphid causes a significant reduction in growth (Dixon, 1971) which is an indication of plant stress (Grime, 1979) makes perfect sense. 

Relationship between mean combined aphid load and the number of sycamore fruit produced the following year.

Instead of mean aphid load, perhaps we ought to be thinking about aphid occurrence at crucial times of the year for the tree, for example budburst. If you go back to the top of the page and look at the photograph of the infested buds you can see that there can be a huge number of aphids present at this time of year just when the trees are starting to wake up and put on new growth. Any interference to the uptake of nutrients at this phase of their life cycle could be detrimental to fruit production.  One way to measure this is by looking at the date the first aphids appear on the buds in the expectation that the earlier the aphids start to feed, the bigger their impact on the trees. Sure enough, the earlier the aphids start feeding, the lower the number of fruit produced.

Significant negative relationship between date of first appearance of aphids on the buds and number of fruit produced in spring.

Although all the relationships I have discussed and shown are significant, the amount of variation is explained is pretty low (over 20% but less than 30%). The relationship that explains most of the variation in any one year is the size of the tree, the bigger the tree the more fruit it produces.

Relationship between size of sycamore tree and number of fruit produced (2009).

As a rule of thumb, the bigger a tree the older it is and older trees have more resources and can afford to produce more offspring than younger smaller trees.

In conclusion, what I can say with confidence is that there is significant variability in sycamore fruit production between years and this is, in my opinion, evidence of masting events, and may be linked to the size and timing of aphid load but is moderated by the size and age of the trees. If you have any other suggestions please feel free to add them in the comments.

If anyone is interested in delving into the data in more depth I will be very happy to share the raw data and also the local weather data for the site.


Binggeli P. (1990) Detection of protandry and protogyny in sycamore (Acer pseudoplatanus L.) from infructescences. Watsonia,18, 17-20.

Binggeli P. (1992) Patterns of invasion of sycamore (Acer pseudoplatanus L.) in relation to species and ecosystem attributes. D.Phil. Thesis, The University of Ulster.

Burt, A. & Bell, G. (1991) Seed production is associated with a transient escape from parasite damage in American beech.  Oikos, 61,145–148.

Dixon, A.F.G. (1971) The role of aphids in wood formation. 1. The effect of the sycamore aphid, Drepanosiphum platanoides (Schr.) (Aphididae) on the growth of sycamore. Journal of Applied Ecology, 8, 165-179.

Hilton, G.M. & Packham, J.R. (1997) A sixteen-year record of regional and temporal variation in the fruiting of beech (Fagus sylvatica L.) in England (1980-1995). Forestry, 70, 7-16.

Hilton, G.M. & Packam, J.R. (2003) Variation in the masting of common beech (Fagus sylvatica L.) in northern Europe over two centuries (1800-2001). Forestry, 76, 319-328.

Janzen, D. H. (1971) Seed predation by animals. Annual Review of Ecology and Systematics, 2,465–492.

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

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

Moreira, X., L. Abdala-Roberts, Y. B. Linhart, and K. A. Mooney. (2014_. Masting promotes individual- and population-level reproduction by increasing pollination efficiency.Ecology, 95, 801–807.

Grime ., J.P. (1979) Primary strategies in plants, Transactions of the Botanical Society of Edinburgh, 43,2, 151-160.

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


Filed under Aphidology, EntoNotes

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.



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.

** 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.)



Filed under Aphidology, Aphids

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 6th 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 21st 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.



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.



Filed under EntoNotes, Roundabouts and more

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

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

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

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

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

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

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

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

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

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

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

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

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


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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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Filed under Ten Papers That Shook My World

Not all aphids aggregate in clumps

There is a tendency for people when they do think of aphids, to see them as existing in large unsightly aggregations, oozing sticky honeydew, surrounded by their shed skins and living in positively slum-like conditions. The bird cherry-oat aphid, Rhopalosiphum padi, the black bean aphid, Aphis fabae, the Poa-feeding aphid, Utamphorophora humboldti and the beech wooly aphid, Phyllaphis fagi, being notable examples.

       Damage on bird cherry             Aphids on runner beans 2014           Office aphids compressed           Beech aphid

Whilst this may be true for many pest aphid species, it is far from true for the group as a whole. Yes they may occur in aggregations, but quite often, they look very neat and tidy and well-behaved.

Conker aphids 2013     Aphids on heath

Some aphid species lead quite solitary lives and you often only find them in ones and twos, if at all, e.g. Monaphis antennata.  There is one aphid species, however, that manages to have it both ways, living surrounded by its friends and relatives but managing to exist in splendid isolation at the same time. The exemplar of this phenomenon is the sycamore aphid, Drepanosiphum platanoidis, which exhibits a behaviour termed ‘spaced-out gregariousness’, a term coined by John Kennedy and colleagues in 1967, although the phenomenon was

sycamore aphids on leaf

described and measured by Tony Dixon a few years earlier. Effectively, the aphids like to be in a crowd but to have their own personal space. As proof of this, when the numbers of aphids on a leaf are low, say two to three, they will, instead of spreading out across the leaf, still show the same behaviour, i.e. get to within 2-3 millimetres distance of each other.

Sycamore compressed

Even more extraordinary is when a predator such as a ladybird or lacewing larvae finds its way on to a crowded leaf; the sycamore aphids do a great imitation of the parting of the Red Sea, but still without touching each other and keeping their regulation distance apart. Those finding themselves at the edge, either take wing or move to the upper surface of the leaf. Although a video of this exists somewhere I have been unable to find it so you will have to take my word for it. If anyone does come across the footage please let me know.

Yet another reason to love aphids.



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

Kennedy, J.S., Crawley, L., & McLaren, A.D. (1967) Spaced-out gregariousness in sycamore aphids Drepanosiphum platanoides (Schrank) (Hemiptera, Callaphididae). Journal of Animal Ecology, 36, 147-170.

Post script 

You may have noticed that the two references cited spell the species name of the sycamore aphid as platanoides,  It is in fact correctly spelt platanoidis.  To their embarrassment both John Kennedy and Tony Dixon got it wrong.  It wasn’t until 1978, when a very brave (possibly helped by conference alcohol consumption) PhD student (David Mercer) of Tony Dixon’s pointed this out, that the error was noticed and corrected 😉


Mercer, D.R. (1979) Flight Behaviour of the Sycamore Aphid, Drepanosiphum platanoidis Schr.   Ph.D Thesis, University of East Anglia, Norwich, UK.



Filed under Aphidology, Aphids

Aphid life cycles – bizaare, complex or what?

In a very early post I mentioned that one of the reasons that I love aphids so much is their life-cycles https://simonleather.wordpress.com/aphidology/  and the fantastic jargon that is used to describe them.  Many undergraduates find the jargon off-putting but it was this complexity that really grabbed my imagination.

aphid jargon

Insects are probably the most diverse group of organisms on Earth (Grimaldi & Engel, 2005) and their life cycles range from simple sexual and asexual styles to complex life cycles encompassing obligate and facultative alternation of sexual and asexual components.  Nancy Moran (1992) suggests that in the insect world probably the most intricate and varied life cycles are found in aphids and I certainly wouldn’t disagree.

There are basically two types of aphid life-cycles, non-host alternating (autoecious, monoecious) and host alternating (heteroecious).   Autoecious aphids spend their entire life cycle in association with one plant species as shown below (Dixon, 1985).

autoecious lifecycle

(or group of related plant species), whereas heteroecious aphids divide their time between two very different species of host plant, usually a tree species (the primary host) on which they overwinter, and an herbaceous plant species (the secondary host) on which they spend their summer.


Approximately 10% of aphid species are heteroecious.  The ancestral aphid life cycle is thought to have been winged, egg laying and autoecious on a woody host plant almost certainly conifers and the oldest families of woody angiosperms e.g. Salicaceae (Mordwilko, 1928; Moran, 1992).

aphid life cycle evolution

Aphid life cycles can also be described as holocyclic, in which cyclical parthenogenesis occurs, with aphids reproducing sexually in the autumn to produce an overwintering egg, in temperate regions and parthenogenetically during spring and summer as shown below for the sycamore aphid (Dixon, 1985).


Some aphids are anholocyclic where the clone is entirely asexual reproducing by parthenogenesis throughout the year. This is often seen in locations where winter conditions are mild, in the tropics for example or as a bit of an oddity around hot-springs in Iceland.


Parthenogenesis in aphids is coupled with live births and reduced generation times through the phenomenon of telescoping generations.  Parthenogenesis in aphids developed early on but whether the oldest aphids (200 mya) were parthenogenetic is not known.

Host alternation appears to have arisen more than once (Moran, 1988), and occurs in four slightly different forms depending on the taxon in which it occurs.  The main differences being in whether the sexual forms are produced on the primary (winter) host (the host on which the eggs are laid), or as in the case of the Aphidini, the males being produced on the secondary (summer) host and the sexual females produced on the primary host.   The majority of aphids host alternate between unrelated woody and perennial hosts, but some species host alternate between herbaceous plants e.g. pea aphid Acyrthosiphon pisum alternates between the perennial vetches and the annual peas Pisum sativum (Muller & Steiner, 1985) and Urleucon gravicorne alternates between the perennial Solidago and the annual Erigeron (Moran 1983).  Some aphid species such as Rhopalosipum padi, have clones that are holocyclic and some that are anholocyclic, so hedge their bets and also gives me the opportunity to slip in a great slide kindly lent to me by my friend Richard Harrington at Rothamsted Research.


One of the things that is rather puzzling is why some aphid species should have adopted a host alternating life cycle which on the face of it, seems to be rather a risky strategy.  You could liken it to looking for a needle in a hay-stack; only about 1 in 300 aphids that leave the secondary host at the end of summer are likely to find their primary host (Ward et al, 1998).  There are a number of theories as to why it has evolved.

1. The nutritional optimization through complementary host growth hypothesis states that heteroecy has been favoured by natural selection because it enables a high rate of nutrient intake throughout the season (Davidson, 1927; Dixon, 1971).  In essence, the clone moves from a host plant where food quality is low and moves onto a herbaceous host that is growing rapidly and thus provides a good source of nutrition.  In autumn, the clone moves back to its primary woody host where leaves are beginning to senesce and provide a better source of nutrition as seen below (Dixon, 1985).

Nutritional changes

On the other hand, non-host alternating aphids such as the sycamore aphid, Drepanosiphum platanoidis, or the maple aphid, Periphyllus testudinaceus, reduce their metabolism and tough it out over the summer months when the leaves of their tree hosts are nutritionally poor, the former as adults, the latter as nymphs (aphid immature forms) known as dimorphs. Mortality over the summer in these species is, however, very high.  In some years I have recorded almost 100% mortality on some of my study trees, so very similar to the 99.4% mortality seen in the autumn migrants (gynoparae) of the bird cherry-oat aphid, Rhoaplosiphum padi.  Other autoecious aphids are able to track resources if they live on host plants that continue to develop growing points throughout the summer.

 Tough it out

Verdict:  No apparent advantage gained

2. The oviposition site advantage hypothesis states that primary woody hosts provide better egg laying sites and provide emerging spring aphids with guaranteed food source (Moran, 1983).  There is however, no evidence that eggs laid on woody hosts survive the winter better than those laid in the herbaceous layer.  Egg mortality in both situations ranges from 70-90% (Leather, 1983, 1992, 1993).

Verdict:  No apparent advantage gained

3.  The enemy escape hypothesis states that by leaving the primary host as natural enemy populations begin to build up and moving to a secondary host largely devoid of enemies confers an advantage on those species that exhibit this trait (Way & Banks, 1968).  At the end of summer, when the natural enemies have ‘found’ the clone again, the clone then migrates back to its primary host, which theoretically is now free of natural enemies.  This is an attractive idea as it is well known that natural enemies tend to lag behind the populations of their prey.

Enemy escape

Verdict: Possible advantage gained

4. The Rendez-vous hosts hypothesis suggests that host alternation assists mate location and enables wider mixing of genes than autoecy (Ward, 1991; Ward et al. 1998).  This seems reasonable, but as far as I know, no-one has as yet demonstrated that host-alternating aphid species have a more diverse set of genotypes than non-host alternating aphids.

Verdict:  Not proven

5.  The temperature tolerance constraints hypothesis which postulates that seasonal morphs are adapted to lower or higher temperatures and that they are unable to exist on the respective host plants at the ‘wrong time of year’ (Dixon, 1985).  I don’t actually buy this one at all, as I have reared spring and autumn morphs at atypical temperatures and they have done perfectly well (Leather & Dixon, 1981), the constraint being the phenological stage of their host plant rather than the temperature.  In addition, there are some host alternating aphid species in which the fundatrix can exist on both the secondary and primary hosts (if the eggs are placed on the secondary host).  This has been experimentally demonstrated in the following species:

Aphis fabae                                 Spindle & bean                                        Dixon & Dharma (1980)

Cavariella aegopdii

Cavariella pastinacea              Willows and Umbelliferae                     Kundu & Dixon (1995)

Cavariella theobaldi

Metopolophium dirhodum       Rose and grasses                                    Thornback (1993)

Myzus persicae                           Prunus spp &  40 different plants       Blackman & Devonshire (1978)

Verdict: Unlikely

6.  The escape from induced host-plant defences hypothesis (Williams & Whitham, 1986), which states that by leaving the primary host as summer approaches, the aphids escape the plant defences being mustered against them.  This is only really applicable to those gall aphids where galled leaves are dropped prematurely by the host plant.

Verdict: Special case pleading?

7.  The constraint of fundatrix specialisation hypothesis is that of Moran (1988), who argues that heteroecy is not an optimal life cycle but that it exists because the fundatrix generation (the first generation that hatches from the egg in spring) on the ancestral winter host, are constrained by their host affinities and are unable to shift to newly available nutritionally superior hosts.  Whilst it is true that some host alternating aphids are however, very host specific as fundatrcies, some aphids are equally host-specific as oviparae at the end of the year the constraints of ovipara specialisation

For example, in the bird cherry-oat aphid Rhopalosiophum padi, the fundatrices are unable to feed on senescent leaf tissue of the primary host, their offspring can only develop very slowly on ungalled tissue and all their offspring are winged emigrants (the alate morph that flies from the primary host to the secondary host) (Leather & Dixon, 1981).  The emigrants are able to feed as nymphs on the primary host on which they develop and as adults on their secondary host, but not vice versa (Leather et al., 1983).  The autumn remigrants (gynoparae, the winged parthenogenetic females that fly from the secondary hosts to the primary hosts on the other hand, feed on the secondary host as nymphs but are unable to feed on the primary host as adults (Leather, 1982; Walters et al., 1984).  The black bean aphid shows similar, but less rigid host specificity and whilst there is a distinct preference for the relevant host plant (Hardie et al., 1989), parthenogenetic forms can occur throughout the summer on the primary host (Way & Banks, 1968), particularly if new growth is stimulated by pruning (Dixon & Dharma, 1980). There are also at least two examples of where both the primary and secondary host are herbaceous (see earlier).  In both these cases the fundatrices could exist on both the primary and secondary host plants

Verdict:  Not proven

So what do I think?  For years I was very firmly convinced that the nutritional optimization hypothesis was the obvious answer; after all Tony Dixon was my PhD supervisor 😉  Now, however, having lectured on the subject to several cohorts of students, if I was forced to pick a favourite from the list above, I would do a bit of fence-sitting and suggest a combination of the nutritional optimization and enemy escape hypotheses. What do you think? There are cetainly a number of possible research projects that would be interesting to follow up, the problem is finding the funding 😦


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Filed under Aphidology, Aphids