Tag Archives: overwintering

Data I am never going to publish in peer-reviewed journals

I have got to that stage in my career where retirement is no longer a distant speck on the horizon; something that 20 years ago I never even thought about, but which now I am actually looking forward to reaching. Don’t get me wrong, I have, in the main, enjoyed what I have been paid to do for the last 40 years, but I’m looking forward to a change of pace and a change of priorities. I’m not planning on leaving entomology and ecology, or putting my collecting equipment in a cupboard, throwing my field guides away and burning all my reprints in a huge bonfire. Nor do I plan on deleting my EndNote™ files and database when I retire to our house in Languedoc-Roussillon to sit next to the pool with a never-emptying glass of red wine and gently pickle myself in the sun*. I’m just looking forward to approaching it in a different way; my plan is to stop initiating the writing scientific papers, but instead to expand on the outreach, to blog more and to write books for a wider audience. I want to spread the joys and wonders of entomology to the world, and hopefully, supplement my pension a bit to make sure that I can keep that glass filled with red wine and heat the swimming pool in the winter 🙂

I’m planning a gradual retirement, a slow(ish) canter towards the day (September 30th 2020) when I finally vacate my university office and move full-time into my converted attic in the Villa Lucie surrounded by my books and filing cabinets with a superb view of the mountains.


The view from my study to be – I will have to stand up to see it, but exercise is good for you 🙂

I have already reached a number of milestones, I took on my last ever PhD student (as Director of Studies) this month (June 7th) and submitted my final grant application as a PI (June 10th).


I must admit that it is a bit of funny feeling, but a remarkably rewarding one in many ways. I look at my former colleagues who have already retired productively and enjoyably, and I’m envious, so I know that I am making the right decision despite the slight feeling of apprehension. I now have a dilemma. As Jeff Ollerton points out, when you have been around a while, in my case it is almost 40 years since I started my PhD**, you build up a substantial amount of data, especially, if as I have, you have supervised over 150 undergraduate research projects, an equal number of MSc research projects and over 50 PhD students. Much of these data are fragmentary, not significant or even lost (sadly when I moved from Imperial College, they threw away the hard copies of my undergraduate projects, although I can remember what some of the lost data were about). My ten year sycamore and bird cherry aphid field study from my time in Scotland (1982-1992) remains largely unpublished and my huge twenty year sycamore herbivores data set from Silwood Park (1992-2012) is in the same boat, although parts of the data are ‘out on loan’ to former students of mine and I hope will be analysed and published before I retire.

This leaves however, the data, some of it substantial, which I would like to see the light of day, e.g. a whole set of rabbit behaviour data that I collected one summer with the help of an undergraduate and MSc student, which surprisingly revealed novel insights. Other data, perhaps not as novel, may be of interest to some people and there is a whole bunch of negative and non-significant data, which as Terry McGlynn highlights over on Small Pond Science, does not necessarily mean that it is of no use.   I have, as an example of fragmentary, not entirely earth-shattering data, the following to offer. Whilst monitoring aphid egg populations on bird cherry and sycamore trees, in Scotland between 1982 and 1992, I occasionally sampled overwintering eggs of Euceraphis betulae, on some nearby birch (Betula pendula) trees and of Tuberculoides annulatus, on an oak tree (Quercus robur) in my back garden in Peebles.

As far as I know there are no published data on the overwintering egg mortality of these two aphids. Although novel for these two aphid species, the observation of the way the egg populations behave over the winter and the factors causing the mortality have already been described by me for another aphid species (Leather, 1980, 1981). I am therefore unlikely to get them published in any mainstream journal, although I am sure that one of the many predatory journals out here would leap at the chance to take my money and publish the data in the Journal of Non-Peer-Reviewed Entomology 🙂 I could of course publish the data in one of the many ‘amateur’ type, but nevertheless peer-reviewed journals, such as Entomologist’s Monthly Magazine, The Entomologist’s Record, The Entomologist’s Gazette or the British Journal of Entomology & Natural History, which all have long and distinguished histories, three of which I have published in at least once (Leather & Brotherton 1987, Leather, 1989, 2015), but which have the disadvantage of not being published with on-line versions except for those few issues that have been scanned into that great resource, The Biodiversity Heritage Library, so would remain largely inaccessible for future reference.

I thus offer to the world these data collected from four Betula pendula trees in Roslin Glen Nature Reserve in Scotland between 1982 and 1986. On each sampling occasion, beginning at the end of October, 200 buds were haphazardly selected and the number of eggs present in the bud axils recorded. Sampling continued until egg hatch began in the spring.


Figure 1. Mean number of eggs per 100 buds of the aphid Euceraphis betulae present on four Betula pendula trees at Roslin Glen Nature Reserve Scotland***.

The number of eggs laid on the trees varied significantly between years (F = 20.3, d.f. = 4/15, P <0.001) ranging from 12.75 eggs/100 buds in 1983-84 to 683 eggs/100 buds in 1986-87. Mortality occurred at a regular rate over the winter and ranged from between 60% in 1985-86 to 83 % in 1984-85, averaging out at 74% over the five-year study.

So in conclusion, no startling new insights, but just some additional data about aphid egg mortality to add to the somewhat sparse records to date (Leather, 1992). Perhaps it is time for me to write another review 🙂


Leather, S.R. (1980) Egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 27, 96-97.

Leather, S.R. (1981) Factors affecting egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 30, 197-199.

Leather, S.R. (1986) Insects on bird cherry I. The bird cherry ermine moth, Yponomeuta evonymellus (L.). Entomologist’s Gazette, 37, 209-213.

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. (1992) Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis, 17, 101-113.

Leather, S.R. (2015) An entomological classic – the Pooter or insect aspirator. British Journal of Entomology & Natural History, 28, 52-54.


*although in light of the recent horrific BREXIT vote this may now not be as simple as it might have been 😦

**I must confess that I haven’t actually published all the data that I collected during my PhD. I rather suspect that this will never see the light of day 🙂

***Data from 1986-87 are not shown as their inclusion makes it very difficult to see the low years. I can assure you however, that the mortality rate shows the same patterns as the other years.




Filed under EntoNotes, Science writing

Midwinter Madness – The Snow flea

Between 1982 and 1992 I worked as a research and advisory entomologist for the UK Forestry Commission based at their Northern Research Station just outside Edinburgh. For the first five years of my time there I worked almost exclusively on the pine beauty moth, Panolis flammea. The pine beauty moth is

snowflea 1

a native insect that became a pest of a non-native tree, Pinus contorta, then a tree that was widely planted over northern Britain. The majority of planting in Scotland was in the north and this meant that my study sites were in Sutherland and Caithness and Aberdeenshire. My main experimental forest was west of Aberdeen in the Spey valley (very handy for the whisky trail) in the Elchies block of Criagellalchie Forest.

snow flea 2

My experimental forest with nearby distillery marked 😉

In Mid-January 1984, I headed north to do some maintenance on my head capsule collecting funnel traps.

snowflea 3

In those days, snow was a perennial hazard, even in the south of Scotland and as I progressed northwards the drifts at the side of the road became increasingly higher. When I reached the forest gates, it was obvious that I was not going to be able to drive to my site. The sun was shining, the sky was blue and the snow glistened. A perfect day for a walk, albeit one of 10 km. Luckily, the weather had been sunny for the last couple of days so the snow was mostly hard enough to walk on. Only in a few places did I break the surface and find that I was standing on about a metre depth of snow. Two hours later as I was approaching my field site, squinting against the sun bouncing off the white untouched snow, I saw black spots moving on the surface. My immediate thought was that I was suffering the first stages of snow-blindness, but as I got nearer I saw that the black dots were actually insects. At first sight I thought I was hallucinating, was this some strange bizarre form of life perhaps an aphid-fly hybridization experiment gone wrong? On closer examination I realised that I was looking at wingless Mecopterans.

snow flea 4

Male snow flea, Boreus hyemalis http://mecoptera.free.fr/Boreus-hyemalis.html


snow flea 5

Female Boreus hyemalis, note the sting-like ovipositor. http://www.wbrc.org.uk/WORCRECD/32/Bingham–John–Snow_Flea_Boreus_hyemalis.html

Although I was familiar with Scorpion-flies, I had never seen these critters before.

snow flea 6

The aptly named Scorpion fly Panorpa communis : https://commons.wikimedia.org/wiki/File:Scorpion_Fly._Panorpa_communis._Mecoptera_(7837166610).jpg

I collected a few to send off for identification and confirmation and carried on into the depths of the forest to check on my funnels. On returning to civilization a day or so later I sent my specimens off to the Natural History Museum and shortly after was informed that I had they were the snow flea, Boreus hyemalis and that I had extended the recorded range of this particular species, albeit only by a few miles.

snow flea 7

My record – it lasted 10 years as the furthest north before M.S.C. Elliott recorded it in February 1994 in Easter Fearn in the north-west Highlands.

Boreus my record

Distribution of Boreus hyemalis in 1994; my record, then the furthest North.


snow flea 9

Current recorded distribution of Boreus hyemalis – obviously widespread – just lacking people willing to go and look for it in the winter 🙂

So what is a snow flea. It is of course, not a flea, being a Mecopteran or Scorpion fly, albeit non-winged.  In Britain there are three species with wings (in the genus Panorpa), the larvae and adults both being predatory on other insects. The adult snow flea is about 5mm long, and lives among moss on which it feeds as both a larva and adult (Withycombe, 1922, 1926). Interestingly, the BugLife site states that they are predatory in both the larval and adult stage. I am not sure where they got this information as they do not cite a reference and all the published literature I have seen indicates that they are moss feeders (Withycombe, 1922, 1926; Fraser, 1943; Hågvar, 2010). Indeed, Wthycombe (1922) conducted a series of experiments on the larvae and conclusively demonstrated that they were unable to complete their development unless fed on moss, although the adults will apparently also feed on dead insects.

These are true winter-active insects, adults emerging in October and November when they mate and lay their eggs the eggs at the base of moss plants), Polytrichium commune being the preferred host (Fraser, 1943). The eggs start to hatch in November and the larvae forage within the moss clumps, pupating towards the end of the summer, emerging as adults after 6-8 weeks.  The adults, which are wingless, thus come out in the coldest months of the year, usually between October and April.  They are most easily seen when walking or jumping on the snow surface. Considering that the adults are winter-active they have a surprisingly high super-cooling point (-6.5oC) (Sömme & Östbye, 1969), especially when compared with the cereal aphid, Sitobion avenae, which has a super-cooling point of -24oC but rarely survives English winters (Knight & Bale, 1986). The BugLife site wonders “how they (snow fleas) manage to jump up to 5 cm without muscular hind legs” but Burrows (2011) found that their jumping prowess is by virtue of large depressor muscles within the thorax which enables them to jump distances of up to 10 cm with a take-off velocity of 1 m s-1, indicating a force of about 16 times their body weight.  So aptly named in this respect too.

The Snow flea is not found (or at least has not been recorded) in the mild south-west of Britain, seeming to prefer areas with a harsher winter. Climate warming may thus pose a threat for this intriguing and little studied insect. Perhaps it is time for us all to venture out in mid-winter and start scanning the surface of snow drifts in heathland areas for these elusive creatures before it is too late.



Burrows, M (2011) Jumping mechanism and performance of snow fleas (Mecoptera, Boreidae). Journal of Experimental Biology, 214, 2362-2374.

Fraser, F.C. (1943) Ecological and biological notes on Boreus hyemalis (L.) (Mecopt., Boreidae). Journal of the Society for British Entomology, 2, 125-129

Knight, J. D. & Bale, J. S. (1986). Cold hardiness and overwintering of the grain aphid Sitobion avenae. Ecological Entomology 11, 189-197.

Sömme, L. & Östbye, O. (1969) Cold-hardiness in some winter active isnects. Norsk Entomologisk Tidsskrift, 16, 45-48

Withycombe, C. L. (1922). On the life history of Boreus hyemalis L. Transactions of the Entomological Society of London, 1921, 312-318.

Withycombe, C. L. (1926). Additional remarks upon Boreus hyemalis L. Entomologist’s Monthly Magazine, 62, 81-83.


Useful link

For more images and observations see http://www.wbrc.org.uk/WORCRECD/32/Bingham–John–Snow_Flea_Boreus_hyemalis.html



Filed under EntoNotes

Ten papers that shook my world – Way & Banks (1964) – counting aphid eggs to protect crops

The previous papers in this series (Southwood, 1961; Haukioja & Niemelä 1976; Owen & Weigert, 1976), were all ones that had an influence on my post-PhD career. This one in contrast, had a direct effect on my PhD as well as on my subsequent career, and was, I guess, greatly influential in the publication of the first book to deal with the ecology of insect overwintering (Leather, Walters & Bale, 1993). In 1964 Mike Way, one of the early proponents of Integrated Pest Management (in fact considered to be the father of UK IPM), was working on control methods for the black bean aphid, Aphis fabae.

Bean aphids

Mike had recently joined Imperial College from Rothamsted Research Station where he had been leading research on ways to reduce pesticide use by farmers and growers.   During his time at Rothamsted he had worked closely with a colleague, C.J. Banks on the black bean aphid including studies on the overwintering eggs. As they said in the introduction to their paper, published four years after their experiments; “During the British winter A. fabae survives almost exclusively in the egg stage. Egg mortality might therefore be important in affecting size of populations of this species and in predicting outbreaks”. They investigated the effects of temperature and predators on the mortality of the eggs on the primary host, spindle, Euonymus europaeus, and concluded that the levels of mortality seen would not affect the success of the aphids the following spring. By 1968 (Way & Banks, 1968) they had followed up on the idea and began to feel confident that aphid populations on field beans could be predicted from the number of eggs on the winter host; spindle bushes. The publication of this paper stimulated the setting up of a long-term collaborative project monitoring Aphis fabae eggs on spindle bushes at over 300 locations throughout England south of the River Humber, and monitoring aphid numbers in about 100 bean fields per year.   In 1977 the results were finally published (Way et al., 1977) and the highly successful black bean aphid forecasting system was born. This was further refined by using the Rothamsted aphid suction trap data (Way et al., 1981).

This was also the year that I began my PhD at the University of East Anglia, working on the bird cherry-oat aphid, Rhopalosiphum padi. In the course of my preparatory reading I came across Way & Banks (1964) just in time to set up a plot of bird cherry saplings which I monitored for the next three winters, the first winter’s work resulting in my first publication (Leather, 1980). I subsequently went on to develop the bird cherry aphid forecasting system still used in Finland today (Leather & Lehti, 1981; Leather, 1983; Kurppa, 1989).

Finnish aphid forecasts

Sadly, despite the great success of these two systems there has not been a huge take-up of the idea, although the concept has been looked at for predicting pea aphid numbers in Sweden (Bommarco & Ekbom, 1995) and rosy apple aphids in Switzerland (Graf et al., 2006). Nevertheless, for me this paper was hugely influential and resulted in me counting aphid eggs for over 30 years!


Bommarco, R. & Ekbom, B. (1995) Phenology and prediction of pea aphid infestations on pas. International Journal of Pest Management, 41, 101-113

Graf, B., Höpli, H.U., Höhn, H. and Samietz, J. (2006) Temperature effects on egg development of the rosy apple aphid and forecasting of egg hatch. Entomologia Experimentalis et applicata, 119, 207-211

Haukioja, E. & Niemela, P. (1976) Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station, 13, 44-47.

Kurppa, S. (1989) Predicting outbreaks of Rhopalosiphum padi in Finland. Annales Agriculturae Fenniae 28: 333-348.

Leather, S. R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur Angewandte Entomolgie 96: 282-287.

Leather, S. R. & Lehti, J. P. (1981) Abundance and survival of eggs of the bird cherry-oat aphid, Rhopalosiphum padi in southern Finland. Annales entomologici Fennici 47;: 125-130.

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

Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492.

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

Way, M.J. & Banks, C.J. (1964) Natural mortality of eggs of the black bean aphid Aphis fabae on the spindle tree, Euonymus europaeus L. Annals of Applied Biology, 54, 255-267.

Way, M. J. & Banks, C. J. (1968). Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter Euonymus europaeus L. Annals of Applied Biology 62, 177-197.

Way, M. J., Cammel, M. E., Taylor, L. R. &Woiwod, I., P. (1981). The use of egg counts and suction trap samples to forecast the infestation of spring sown field beansVicia faba by the black bean aphid, Aphis fabae. Annals of Applied Biology 98: 21-34.

Way, M.J., Cammell, M.E., Alford, D.V., Gould, H.J., Graham, C.W., & Lane, A. (1977) Use of forecasting in chemical control of black bean aphid, Aphis fabae Scop., on spring-sown field beans, Vicia faba L. Plant Pathology, 26, 1-7.


Post script

Michael Way died in 2011 and is greatly missed by all those who knew him well. He examined my PhD thesis, and to my delight and relief, was very complimentary about it and passed it without the need for corrections. I was greatly honoured that a decade or so later I became one of his colleagues and worked alongside him at Silwood Park. He was a very modest and self-deprecating man and never had a bad word to say about anyone. He had a remarkable career, his first paper published in 1948 dealing the effect of DDT on bees (Way & Synge, 1948) and his last paper published in 2011 dealing with ants and biological control (Seguni et al., 2011), a remarkable 63 year span. His obituary can be found here http://www.telegraph.co.uk/news/obituaries/science-obituaries/8427667/Michael-Way.html


Filed under Aphidology, Aphids, Ten Papers That Shook My World

A Christmas Aphid

A few weeks ago I was contacted by a researcher from the One Show.  They were interested in the possibility of doing a festive piece about what people bring into the house with them on Christmas trees with the idea that George McGavin would shake a Christmas tree over a piece of white paper and tell the audience all about the insects that fell out;  a typical media “how gross nature” is piece.

The researcher was somewhat disappointed when I told her that being winter  that there would be relatively little hiding in the tree, especially if it was a commercially reared cut tree bought from a garden centre or other retail outlet.  Cut Christmas trees in the UK tend to be harvested from October onwards so the chances are that your tree has lain about for at least a month before you bring it into your house and by that time, any sensible winter active herbivore has long departed for fresher trees.  Although conifer trees have a large number of insect species associated with them, most of them spend the winter either off the tree or as inactive eggs hidden under the bark or as eggs actually laid inside the needles e.g. the pine sawfly Neodiprion sertifer.  You would probably find a few opportunistic spiders and possibly some mites and bark lice, but not much else unless you had a potted tree or one that had only recently been felled.  The other thing that would influence what you would find is of course what species of tree you had bought.  Gone are the days when the Christmas tree and Norway spruce (Picea abies) were one and the same.  I guess my caveating and pessimistic reply proved too much for the researcher as I never heard back from her.

The one insect I had waxed lyrical about was of course an aphid, the green spruce aphid, Elatobium abietinum to be precise.   There are a number of aphid species that make a living on spruce trees, some of them quite large and spectacular such as the greater black spruce aphid, Cinara piceae, but like most aphids, they overwinter as eggs (Leather, 1992).


The greater black spruce aphid, Cinara piceae (Photograph courtesy of http://influentialpoints.com/Gallery/Aphids_on_spruce_Picea_in_Britain.htm)

The green spruce aphid, E. abietinum or Elatobium as it is commonly known, (there is only one species in the genus), overwinters in the UK and most other parts of the world, as an adult or immature stage (nymph) (Nicol et al., 1998).

The adult is small, green and inconspicuous, and quite difficult to see unless you are actually looking for them.

Elatobium and nymphs

The green spruce aphid, Elatobium abietinum and nymphs.

The green spruce aphid is a native of Europe and normally attacks Norway spruce.  They avoid current year needles as these tend to be distasteful to them (the chemistry of young spruce needles is pretty nasty and makes them unsuitable hosts for the aphids) and feed on the previous year and older needles.  Spruce needles, even older ones, are not particularly nutritious, so the aphid injects a toxic material in its saliva that makes the needles more nutritious by encouraging nitrogen mobilisation (Kloft & Erhardt, 1959).  Their populations build up during the spring and towards the end of May and beginning of June, they take flight and the trees seem relatively free of aphids (Bevan, 1966).  As they are so small, they are most obvious after they have gone, either by the damage they cause, premature senescence of the needles as shown in the photograph above, premature needle drop or by the presence of a large number of ladybird larvae.  When I worked for the Forestry Commission as an entomologist, I quite often received phone calls from distressed foresters who had sprayed the blue beetles damaging their spruce trees!

Although they are difficult to find during the summer months they are still there; this summer collapse of singe-host aphids is quite common (Karley et al., 2004).  In the autumn,  Elatobium populations begin to build up and as they do not overwinter as eggs, they are able to continue reproducing through the winter months (Powell & Parry, 1976). Sitka spruce, Picea sitchensis, the most commonly grown conifer in the UK, is a native of North America and as such has very low resistance to Elatobium and displays an almost hypersensitive response to the toxic saliva produced by the aphid.

If it is a particularly mild winter then the spruce trees are likely to show severe signs of damage by June and July.  After several mild winters spruce trees may end up with only current year needles present, which has a severe effect on their growth and appearance.

Elatobium damage needles

Branches of Sitka spruce with only current year needles present after a severe Elatobium abietinum infestation

Elatobium damage trees

Sitka spruce trees showing discoloured needles after attack by Elatobium abietinum.

It may be small, inconspicuous and not worth a TV appearance, but  Elatobium abietinum is now a pest with a world-wide distribution and an international reputation.


Bevan, D. (1966). The green spruce aphis Elatobium (Neomyzaphis) abietinum Walker. Scottish Forestry 20, 193-201.

Karley, A. J., Parker, W. E., Pitchford, J. W. &Douglas, A. E. (2004). The mid-season crash in aphid populations: why and how does it occur? Ecological  Entomology 29, 383-388.

Kloft, W. & Ehrhardt, P. (1959). Unterschungen uber Saugtatigkeit und Schadwirkung der Sitkafichtenlaus, Liosomuphis abietina (Walk.), (Neomyzaphis abietina Walk.).  Phytopathologie Zeitzschrqt 35, 401 – 410.

Leather, S. R. (1992). Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis 17, 101-113.

Nicol, D., Armstrong, K. F., Wratten, S. D., Walsh, P. J., Straw, N., Cameron, C. M., Lahmann, C. & Frampton, C. M. (1998). Genetic diversity of an introduced pest, the green spruce aphid Elatobium abietinum (Hemiptera: Aphididae) in New Zealand and the United Kingdom. Bulletin of Entomological Research 88, 537-543.

Powell, W. & Parry, W. H. (1976). Effects of temperature on overwintering populations of the green spruce aphid, Elatobium abietinum.  Annals of Applied Biology 82, 209-219.

Sullivan, C.R. (1965) Laboratory and field investigations on the ability of eggs of the European Pine Sawfly, Neodiprion sertifer (Geoffroy) to withstand low winter temperatures.  Canadian Entomologist, 97, 978-993



During the 1980s when ‘Acid Rain’ was very much in the news, Elatobium damage was often mistaken as a symptom of acid rain in the UK.



Filed under Aphidology, Aphids

A Winter’s Tale – aphid overwintering

Aphids that live in temperate or boreal regions have to be able to survive overwinter. Aphids, depending on species, are able to pass winter in two ways. If they are holocyclic i.e. possess an egg-laying stage, they usually overwinter as eggs. Aphid eggs are extremely cold-hardy; they have been reported to have super-cooling points of about -42oC (Somme ). If laid on a woody host, eggs are usually laid in the bud axils as in the case of the apple aphid, Aphis pomi, the black bean aphid Aphis fabae and the bird cherry aphid, Rhopaloishum padi.

aphid eggs

In some instances, such as the sycamore aphid, Drepanosiphum platanoidis, eggs are laid directly on the tree bark or in crevices in the bark or even in lichen growing on the bark.  See if you can spot the eggs in the picture below.


If however, the aphid in question lives on an herbaceous host, the eggs may be laid directly on the ground, on or amongst fallen leaves or at the base of grass tussock.

The other strategy adopted by those aphids that are anholocyclic, such as the green spruce aphid, Elatobium abietinum, is to pass the winter as an active stage, either as an adult or immature nymph. Those holocyclic aphids that have anholcyclic strains are also able to adopt this strategy. Despite their soft bodies and fragile appearance, aphids have quite low super-cooling points values such as -26oC having been reported (Griffiths & Wratten, 1979).

A potential advantage of using an active overwintering stage and not an egg, is that if they survive the winter, they are able to start reproducing sooner, particularly if they are a host –alternating aphid, where the aphids hatching from eggs, have to spend time developing and reproducing on the primary woody host before being able to migrate to the secondary hosts. This also applies, to a lesser extent, to those holoyclic aphids living on herbaceous plants, although the temporal advantage is not as great. One would assume that given the relative cold-hardiness attributes of aphid eggs and adults that in a country such as the UK where winter temperatures below -10oC are both infrequent and short lasting, winter survival of aphids would be extremely high if not guaranteed. This is not the case. For example, eggs mortality of the bird cherry aphids is typically around 70-80% as shown in my first ever publication (no fancy graphics packages in those days, just Letraset , Indian ink, stencils and tracing paper). Actually people had measured aphid egg mortality much earlier than this (Gillette, 1908) but I was the first person to monitor mortality throughout the winter and show that it occurred at a steady rate irrespective of the severity of the winter.

 Egg survival

It is actually a function of the length of the winter that determines how many eggs survive, the longer the winter the greater the mortality.

Egg mortality

This level of mortality is typical for all aphid species for which I have data (Leather, 1993). Some of this mortality can be attributed to predation, but most of it is intrinsic (Leather, 1981), possibly due to cryo-injury.

Similarly, those aphids that overwinter as adults or nymphs, despite their ability to super-cool to temperatures below -20oC, experience even greater levels of mortality as shown elegantly by Jon Knight and Jeff Bale in 1986 studying overwinter survival of the grain aphid Sitobion avenae near Leeds.

Knight & Bale

In fact one wonders how any aphids at all survive winter this way, but they certainly do if the winters are mild enough, as in the case of Myzus persicae and Sitobion avenae in southern England and E. abietinum throughout most of its range (Day et al., 2010). An interesting anomaly is Iceland where hot springs abound and the bird cherry aphid is able to survive anholocyclically on grasses growing around the springs whereas in other countries with similar winter temperatures it would only be able to survive as the egg stage.

Despite the importance of winter to aphid population dynamics we still know very little about their winter ecology, our knowledge being confined to a handful of economically important species. Despite the discomfort of field work in the winter this is an area which would be very rewarding to anyone in need of an interesting and good research project.  Finger-less mittens are, however, definitely recommended 😉

Useful references

Bale, J. S. (1996). Insect cold hardiness: a matter of life and death. European Journal of Entomology 93, 369-382. http://www.eje.cz/pdfs/eje/1996/03/09.pdf

Day, K. R., Ayres, M. P., Harrington, R. & Kidd, N. A. C. (2010). Interannual dynamics of aerial and arboreal spruce aphid populations. Population Ecology 52, 317-327. http://link.springer.com/article/10.1007/s10144-009-0190-0#page-1

Gillette, C. P. & Taylor, E. P. (1908). A few orchard plant lice. Colorado Agricultural Experimental Station Bulletin, 113, 1-47.

Griffths, E. &Wratten, S. D. (1979). Intra-and inter-specific differences in cereal aphid low temperature tolerance. Entomologia experimentalis et applicata 26, 161-167. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1979.tb02912.x/abstract

Knight, J. D. & Bale, J. S. (1986). Cold hardiness and overwintering of the grain aphid Sitobion avenae. Ecological Entomology 11, 189-197.

Leather, S. R. (1980). Egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata 27, 96-97. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1980.tb02951.x/abstract

Leather, S. R. (1981). Factors affecting egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Ent omologia experimentalis et applicata 30, 197-199. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1981.tb03097.x/abstract

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. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1993.tb01192.x/abstract;jsessionid=9FC2ED8174E96317F192CF42A19092FE.f03t03?deniedAccessCustomisedMessage=&userIsAuthenticated=false

Strathdee, A. T., Howling, G. G. & Bale, J. S. (1995). Cold hardiness of overwintering aphid eggs. Journal of Insect Physiology 41, 653-657. http://www.sciencedirect.com/science/article/pii/002219109500029T


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 😦


Blackman, R.L. & Devonshire, A.L. (1978)  Further studies on the genetics of the carboxylase-esterase regulatory system involved in resistance to orgaophosphorous insecticides in Myzus persicae (Sulzer).  Pesticide Science 9, 517-521

Davidson, J. (1927) The biological and ecological aspects of migration in aphids.  Scientific Progress, 21, 641-658

Dixon, A.F.G. (1971) The life cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi (L) and its bearing on the theory of host alternation in aphids. Annals of  Applied Biology, 68, 135-147.  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1971.tb06450.x/abstract

Dixon, A.F.G. (1985) Aphid Ecology Blackie, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1980.tb02981.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Grimaldi. D. & Engel, M.S. (2005)  Evolution of the Insects, Cambridge University Press, New York

Hardie, J. (1981) Juvenile hormone and photoperiodically controlled polymorphism in Aphis fabae: postnatal effects on presumptive gynoparae. Journal of Insect Physiology, 27, 347-352.

Hardie, J. Poppy, G.M. & David, C.T. (1989) Visual responses of flying aphids and their chemical modification. Physiological Entomology, 14, 41-51.  http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3032.1989.tb00935.x/abstract

Kundu, R. & Dixon, A.F.G. (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology, 64, 245-255.  http://www.jstor.org/discover/10.2307/5759?uid=3738032&uid=2&uid=4&sid=21102533364873

Leather, S.R. (1982) Do gynoparae and males need to feed ? An attempt to allocate resources in the bird cherry-oat oat aphid Rhopalosiphum padi. Entomologia experimentalis et applicata, 31, 386-390.  http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1982.tb03165.x/abstract

Leather, S.R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur  Angewandte  Entomolgie, 96, 282-287. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1983.tb03670.x/abstract

Leather, S.R. (1992) Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis, 17, 101-113.  http://www.cabdirect.org/abstracts/19941101996.html;jsessionid=60EA025C7230C413B6094BCC4966EC06

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. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1993.tb01192.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

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. http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1981.tb05136.x/abstract

Moran, N.A. (1983) Seasonal shifts in host usage in Uroleucon gravicorne (Homoptera:Aphididae) and implications for the evolution of host alternation in aphids. Ecological Entomology, 8, 371-382. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2311.1983.tb00517.x/full

Moran, N.A. (1988) The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. American Naturalist, 132, 681-706. http://www.jstor.org/discover/10.2307/2461929?uid=3738032&uid=2&uid=4&sid=21102533364873

Moran, N.A. (1992) The evolution of aphid life cycles. Annual Review of Entomology, 37, 321-348. http://www.annualreviews.org/doi/abs/10.1146/annurev.en.37.010192.001541

Mordwilko, A. (1928)  The evolution of cycles and the origin of heteroecy (migrations) in plant-lice.  Annals and Magazine of Natural History Series 10, 2, 570-582

Muller, F.P. & Steiner, H. (1985)  Das Problem Acyrthosiphom pisum (Homoptera: Aphididae).  Zietsschrift fur angewandte Entomolgie 72, 317-334

Thornback, N. (1983)  The Factors Determiining the Abundance of Metopolophium dirhodum (Walk.) the Rose Grain Aphid.  PhD Thesis, University of East Anglia.

Walters, K.F.A., Dixon, A.F.G., & Eagles, G. (1984) Non-feeding by adult gynoparae of Rhopalosiphum padi and its bearing on the limiting resource in the production of sexual females in host alternating aphids. Entomologia experimentalis et applicata, 36, 9-12. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1984.tb03398.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Ward, S.A. (1991). Reproduction and host selection by aphids: the importance of ‘rendevous’ hosts. In Reproductive Behaviour of Insects: Individuals and Populations (eds W.J. Bailey & J. Ridsdill-Smith), pp 202-226. Chapman & Hall, London.

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. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2656.1998.00238.x/full

Way, M.J. & Banks, C.J. (1968) Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter host Euonymus europaeus L. Annals of Applied Biology, 62, 177-197.  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1968.tb02815.x/abstract

Williams, A.G. & Whitham, T.G. (1986) Premature leaf abscission: an induced plant defense against gall aphids. Ecology, 67, 1619-1627.  http://www.jstor.org/discover/10.2307/1939093?uid=3738032&uid=2&uid=4&sid=21102533364873


Filed under Aphidology, Aphids

The Curious Case of the Shark-finned Aphid

The large (giant) willow aphid, Tuberlolachnus salignus, is, in my opinion, one of the world’s greatest unsolved mysteries.  This aphid is sometimes regarded as being the largest aphid in the world.  It can reach a length of 5 mm, can weigh up to 13 mg as an adult and the new-born nymphs weigh about 0.25 mg (Hargreaves & Llewellyn, 1978).  You can get an idea of how big it is from the picture below.

willow aphid on finger


This is pretty big for an aphid, although not quite as big as one of my former PhD students (Tilly Collins) liked to pretend!  The picture below used to appear on her website and was the envy of a number of Texan entomologists.  Tuberolachnus salignus, as you might expect, since it feeds through the bark and not on leaves, has rather a long set of stylets, up to  1.8 mm, more than a third of it’s body length (Mittler, 1957).

tilly on aphid

This picture emphasises the first mystery: what is the function of the dorsal tubercle, which so closely resembles a rose thorn, or to me, a shark’s fin.  Nobody knows.  Is it defensive? Unlikely, since T. salignus being a willow feeder is stuffed full of nasty chemicals and very few predators seem to want, or be able to feed on it.  They feed in large aggregations on the stems of their willow tree hosts and can have serious effects on tree growth (Collins et al., 2001).  As the aphids produce a lot of honeydew, they are often ant-attended  (Collins & Leather, 2002) and these also deter potential predators.  In fact the aphid colonies produce so much honeydew in the summer that they attract huge numbers of vespid wasps that are in search of energy-rich sugar sources at that time of year.  These too are likely to make potential predators and parasitoids think twice about approaching the aphids.


Photograph courtesy Dr Tilly Collins

The wasps also cause a problem for researchers and when Tilly was doing her PhD, she used to have to confine her fieldwork to those times of day when the wasps were not around.   In addition, if you crush one of the aphids you will discover that it stains your fingers bright orange and that this stain will last several days if you don’t try too hard to wash it off.  If you get this aphid ‘blood’ on your clothes they will be permanently marked and Tilly used to say that she ought to be paid an extra clothing allowance.

Tuberolachnus salignus, is as far as we can tell, anholocyclic, no males have been recorded and no matter how hard people have tried to induce the formation of males and sexual females, they have not been successful.  This is however, not the second mystery.  The mystery is that every year, in about February, it does a disappearing act and for about four months its whereabouts remain a mystery (Collins et al., 2001).  So we have an aphid that spends a substantial period of the year feeding on willow trees without leaves and then in the spring when most aphids are hatching from their eggs to take advantage of the spring flush, T. salignus disappears!  Does it go underground?  If so, what plant is it feeding on and why leave the willows when their sap is rising and soluble nitrogen is readily available?

So here is a challenge for all entomological detectives out there.  What is the function of the dorsal tubercle and where does T. salignus go for the spring break?

Truly a remarkable aphid and two mysteries that I would dearly love to know the answers to and yet another reason why I love aphids so much.

Collins, C.M. & Leather, S.R. (2002) Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality. Ecological Entomology, 27, 238-241. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2311.2002.00390.x/full

Collins, C. M., Rosado, R. G. & Leather, S. R. (2001). The impact of the aphids Tuberloachnus salignus and Pterocomma salicis on willow trees. Annals of Applied Biology 138, 133-140 http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.2001.tb00095.x/abstract.

Hargreaves, C. E. M. & Llewellyn, M. (1978). The ecological energetics of the willow aphid, Tuberolachnus salignus:the influence of aphid Journal of Animal Ecology, 47, 605-613. http://www.jstor.org/discover/10.2307/3804?uid=3738032&uid=2&uid=4&sid=21101920521473

Mittler, T. E. (1957). Studies on the feeding and nutrition of Tuberolachnus salignus (Gmehn) (Homoptera, Aphididae). I. The uptake of phloem sap. Journal of  Experimental Biology, 34, 334-341  http://jeb.biologists.org/content/34/3/334.full.pdf

Other resources




Filed under Aphidology, Aphids, EntoNotes