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Aphids galore, les pucerons à gogo – UK-France Joint Meeting on Aphids – April 3rd to 5th 2019

The giant aphid – a fitting start to an aphid conference, albeit taxonomically suspect 😊

I have just returned from a very enjoyable two-day meeting at Rothamsted Research Station in Harpenden.  This was a follow-up to the very enjoyable meeting we had in Paris in 2015 which made me ask somewhat facetiously, if pea aphids ruled the world 😊 As with the Paris meeting, this recent meeting was jointly organised by Jean-Christophe Simon and Richard Harrington with some input by me.  There were ninety delegates, and not just from France and the UK; we had a keynote speaker from Japan, Tsutomu Tsuchida, and also speakers from Belgium, the Czech Republic, Germany, Ireland and Switzerland.

Tsumato Tsuchida, me, Richard Harrington, Julie Jaquiéry, Jean-Christophe Simon and Richard Blackman.

Our other three keynote speakers included two of the doyens of the aphid world, Roger Blackman and Helmut van Emden   and Julie Jaquiéry from the University of Rennes.  As with the Paris meeting, many of the talks were about the pea aphid and symbionts.  Other aphids did, however, get mentioned, including my favourite aphid, Rhopaloisphum padi, which featured in an excellent talk by PhD student Amma Simon from Rothamsted, who is supervised by one of my former students, Gia Aradottir.  There was an excellent poster session, a tribute to the late great, Ole Heie from Mariusz Kanturski, a fabulous film by Urs Wyss, which included shocking scenes of lime aphids being torn apart by vicious predators, and of course the conference dinner.

It would take too long to describe all the talks, so I will let the pictures tell the story of a very enjoyable meeting.  Hopefully we will all meet again in France in 2023.

Great talks and a packed lecture theatre

Food and chat

Very animated poster sessions

Three senior aphidologists in action,  Helmut Van Emden, Hugh Loxdale and Roger Blackman

Richard Harrington presenting Roger Blackman and ‘Van’ van Emden with the Award of the Golden Aphid – the lighting in the conference dining area was very peculiar 😊

Strange lighting at the conference dinner

From the Urs Wyss film– lime aphid moulting

The giant aphid having a quick snack

And in case you wondered, there were embryos inside the giant aphid 🙂

Many thanks to the Royal Entomological Society and BAPOA/INRA for funding.

And here are most of the delegates on the final day

Aphid SIG 2019

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Entomological classics – the Light Trap

I think that even those of us who are not entomologists are familiar with the attraction that insects, particularly moths, have for light. The great Sufi philosopher Bahauddin Valad (1152-1231) wrote the following lines

a candle has been lit

inside me,

for which

the sun

is a moth.

 

In Shakespeare’s The Merchant of Venice (1596), Portia famously declaims “Thus hath the candle singed the moath.”

Moths and flame

It may thus come as a bit of surprise to realise that ‘modern’ entomologists were quite slow to develop bespoke traps that took advantage of this aspect of insect behaviour. That said, according to Beavis (1995) the Roman author Columella (Lucius Junius Moderatus, 4-7 AD), describes a light trap to be used to protect bee hives from wax moth attacks. A pretty much identical trap was still being used in 1565 (Gardiner, 1995) although he erroneously calls it the first light-trap. As far as I can tell the early ‘modern’ Lepidopterists used the white sheet technique, still used today, where a light source such as a paraffin lamp (nowadays an electric light or powerful torch) was suspended above or behind a white sheet, from which the intrepid entomologist collected specimens of interest that come to rest on the sheet. This can be very efficient but does require the entomologist to be ‘on duty’ throughout the trapping

White sheet

The white sheet technique.

period, although on a fine night, with good companionship and an ample supply of beer, or other alcoholic beverage, it can be a very pleasant way to spend a long evening 😉

The earliest published reference to a modern bespoke light trap that I have been able to find is a patent from 1847 for a modified beehive which includes a light trap to lure wax moths away from the main part of the hive (Oliver Reynolds, 184, US Patent5211; http://www.google.com/patents/US5211).

Reynolds beehive 3

The modified Reynolds Beehive incorporating moth trap.

The second published reference to a bespoke light trap is again one designed to control wax moths and is described in a patent application by J M Heard dated 1860. In this case as far as I can make out the lamp is actually glass coated with a phosphorescent material rather than using a candle or oil flame.

Figure 4

“The basin A, is supplied with a requisite quantity of molasses or other suitable substance to serve as a bait, and the inner sides of the glass plates c, of the lamp C, are covered with a mixture of phosphorus and oil or phosphorus combined with any suitable substance to form a cement, or a stick E, may be coated with the cement, said stick being passed through the tube e, into the lamp, as shown plainly in Fig. 1. The insects decoyed by the light and attracted by the bait, strike against the inclined glass plates c, and fall into the basin A. By having the plates c, inclined the insects are made to fall through the opening b, into the basin and said opening is permitted to be comparatively small and the cover a, of the basin in connection with the cover D, of lamp protect perfectly the bait from sun and rain, thereby protecting an unnecessary waste of the same. During the day the phosphorus of course is not needed unless it be cloudy, but the device is chiefly efficacious at night as the visits of the insects are mostly nocturnal.”

So whilst beekeepers and agriculturalists were busy using traps to attract moths to kill them what were the lepidopterists doing? It appears that they were using whole rooms as light traps as described here by H T Stainton in 1848.

Figure 5

 

A later Victorian entomological ‘how to’ book, added instructions of how to use gas and paraffin lamps outside, with the lepidopterist standing ready with his net (Greene, 1880).

The 20th Century was however, when we see the birth of the light traps as we know them today. First on the scene was the Rothamsted Trap, developed by the great C B Williams, which was

 

Rothamsted electric 6

The electric ‘fixed’ Rothamsted Trap.

Rothamsted portable 7

The ‘portable’ Rothamsted Trap – Williams (1948)

developed from earlier versions that he used in the 1920s and 1930s, in Egypt and England (Williams, 1924, 1935).

Rothamsted colour 8

Rothamsted trap in action

 

Apparently the first electrical light trap to use an ultra-violet light was made in 1938 (Barratt, 1989) and used in the 1940s (Fry & Waring, 2001) but it was not until 1950 that the first commercially available version was produced (Robinson & Robinson, 1950).

Robinson 9

The Robinson Trap – very popular and ideal for use in gardens where there is easy access to a mains supply.

 

Strangely, considering that the Americans had been first on the scene with patented light traps it was not until 1957 that the Pennsylvanian and Texas traps appeared on the scene (Frost, 1957) closely followed by the Texas traps (Hollingsworth et al., 1963). These traps used fluorescent tubes instead of bulbs and were particularly good at catching beetles, moths and ants. The Texas trap and the Pennsylvania trap were essentially the same, the main difference being that the Pennsylvania trap has a circular roof to prevent train entering the killing bottle. As Southwood (1966) somewhat tongue in cheek says, this may reflect the differences in the climate of the two states 😉

Pennyslvania 10

The Pennsylvanian Light Trap.

In the 1960s the Heath Trap appeared on the scene (Heath, 1965). This was billed as being extremely portable, being able to be carried in a back pack and also able to be run either from a mains supply or from a 12 volt battery.

Heath 11

The Heath Light trap.

Less expensive and more portable is the Skinner trap, (designed by Bernard Skinner in as far as I can make out in the early 1980s, please let me know if you know exactly) which comes in wooden and aluminium versions and is collapsible, so that if needed, several can be transported at once. It comes in both mains and battery versions.

Skinner elctric 12   Skinner portable 13

The Skinner light trap – relatively inexpensive and very portable.

An interesting combination of light and odour being used to attract and trap insects, in this case to ‘control’ them, is the Strube Stink bug trap. This is an American invention and is used to protect US householders against the the Brown Marmorated Stink Bug, Halyomorpha halys, an invasive species from Asia which appears to have developed a propensity to overwinter in people’s houses. I remember a few years ago that we in the UK were warned that it might cross the channel from France; this resulted in lurid headlines in the ‘Red Top’ newspapers with wording like ‘stench spraying insect’ being used 😉

Straub 14

Strube Stink Bug Trap

 

This appears to be a very effective trap; all the reviews I have read praise it highly, so if the Brown Marmorated Stink Bug does make it to the UK, the Strube trap will be the one to buy!

 

References

Frost, S.W. (1957) The Pennsylvanian light trap. Journal of Economic Entomology, 50, 287-292.

Fry, R. & Waring, P. (2001) A Guide to Moth Traps and their Use. Amateur Entomologist, Orpington, Kent.

Gardiner, B.O.C. (1995) The very first light-trap, 1565? Entomologist’s Record and Journal of Variation, 107, 45-46

Greene, J. (1880) The Insect Hunter’s Companion. W. Swan Sonnenschein & Allen, London.

Heath, J. (1965) A genuinely portable MV light trap. Entomologist’s Record and Journal of Variation, 77, 236-238.

Hollingsworth, J.P., Hartstock, J.G. & Stanley, J.M. (1963) Electrical insect traps for survey purposes. U.S.D.A. Agricultural Research Service 42-3-1, 10 pp.

Robinson, H.S. & Robinson, P.J.M. (1950) Some notes on the observed behaviour of Lepidoptera in the vicinity of light sources together with a description of a light trap designed to take entomological samples. Entomologist’s Gazette, 1, 3-20

Southwood, T.R.E. (1966) Ecological Methods. Chapman & Hall, London

Stainton, H.T. (1848) On the method of attracting Lepidoptera by light. The Zoologist, 6, 2030-2031

Williams, C.B. (1924) An improved light trap for insects. Bulletin of Entomological Research, 15, 57-60.

Williams, C.B. (1935) The times of activity of certain nocturnal insects, chiefly Lepidoptera, as indicate by a light-trap. Transactions of the Royal Entomological Society of London B, 83, 523-555.

Williams, C.B. (1948) The Rothamsted light trap.   Proceedings of the Royal Entomological Society of London A, 23, 80-85.

 

Post script

There are of course more light traps out there, many being variations of those described above, or for specific insect groups such as mosquitoes or aquatic traps for Cladocera (water fleas). Many ‘home made’ traps also exist, such as the ‘portable’ one I made for use on the field course that I used to run at Silwood Park.

Leather 15

The Leather Light Trap

I used a rechargeable battery lantern, but other light sources would also work. In retrospect I should have painted the Perspex black so that only the ‘entrance’ funnels emitted light. There was a tendency for insects to sit on the outside of the trap rather than enter it.

A useful link for those wishing to make their own traps can be found here http://www.theskepticalmoth.com/techniques/light-traps/ and Fry & Waring (2001) also has some very useful hints and tips.

 

 

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The Scent of Fear – the aphid alarm pheromone

We are all familiar with the effects of epinephrine (adrenaline) and norepinephrine (noradrenaline) on us when placed in a position of stress, such as public speaking or even worse danger.  We flush, shake, our heart rate accelerates and many of us we begin to sweat profusely, thus visibly advertising our distress; sometimes embarrassingly so

Sweating nervously

 

if we have an antiperspirant  fail and happen to be wearing a dark shirt.

man_giving_speech

http://www.silkyskin.co.uk/blog/wp-content/uploads/2012/07/man_giving_speech.jpg

Those seeing these symptoms may feel a degree of sympathy for the victim, but do not usually flee the scene, although they may sometimes feel tempted to do so.

The case with aphids is very different.   Aphids, when perceiving a threat to their neighbours by a predator or parasite, flee the scene rapidly, by flight, if winged, on foot if not, or even by leaping from their host-plant to the ground below.  The pea aphid, Acyrthosiphon pisum walks away or drops from their plant (Clegg & Barlow, 1982) as does the rose-grain aphid, Metopolophium dirhodum (Larsen, 1988).  This may seem a risky move since it seems that about 10% of all aphids that fall from their host plant don’t manage to get back (Sunderland et al., 1986), but for a clonal organism the risk is obviously worth it.

So how does this communal fright and flight response come about?  Most aphids have a pair of siphunculi or cornicles at the rear of their abdomen.  These vary in size and shape, in some aphids being long and slender, in others short and stubby and in yet others reduced to a shallow indentation (pore) or in a few species, totally absent.

Siphunculi

The role of aphid siphunculi has been debated since the days of Linneaus and Reaumur who considered them to be the source of honeydew (Hottes, 1928).  Hottes himself in a comprehensive review of the various theories put forward for the function of the siphunculi, dismissed the defence theory of Busgen (1891) and plumped for an excretory role, although he did suggest that volatile substances were produced by the siphunculi in addition to the waxy visible drops.    By the middle of the last century it was generally accepted that the siphunculi were involved in defence, but in a purely physical way, in that the waxy exudate was used to deter or disable the attacking predators or parasites (e.g. Dixon, 1958; Edwards, 1966).  At about the same time, the chemical composition of the visible exudate was confirmed as being primarily triglycerides with myristic acid being the major fatty acid present (Strong, 1966).

Oleander Aphid- Milkweed-- Mark Bower - 1 - 1

Aphis nerii siphuncular exudate.  http://springfieldmn.blogspot.co.uk/2014/08/aphid-cornicles.html

 

 

Hawthorn-parsley aphid Dysaphis apiifolia producing sipuncular exudates whilst under attack by a parasitic wasp.  Many thanks to Tom Pope for permission to use this clip.

In 1968 an alarm pheromone was identified and isolated from the cotton stainer, Dysdercus intermedius (Calam & Youdeowei, 1968) so it was not surprising that attention should be focused on aphids, many of which show a similar group dispersive behaviour when a predator approaches them.   The aphid alarm pheromone (E)-β-farnesene was, however, not formally identified until  1972 (Bowers et al, 1971), although Maria Dahl had demonstrated the  previous year that a solution made from crushed aphids would cause an alarm response in other aphids of the same and different species (Dahl, 1971). Unsurprisingly, as during the 1970s and 1980s scientists from the USA were notorious for only citing papers written in English, Bowers et al. (1972), failed to cite her in their paper, instead citing two other American authors (Kislow & Edwards, 1972).

This discovery resulted in a flurry of papers from around the world as insect physiologists vied to be the first to isolate alarm pheromone from different aphid species (e.g. Weintjens et al., 1973; Montgomery & Nault, 1977; Wohlers, 1980).  There were also more ecological studies such as that examining the way alarm pheromone in ant-attended aphids enhances the relationship between them and their ant farmers (Nault et al., 1976) thus acting as a synomone (Nordlund & Lewis, 1976).  As time has gone on the interest in aphid alarm pheromone has remained unabated with new twists and surprises being discovered.  For example, as well as stimulating the escape response, the alarm pheromone also stimulates those surviving pea aphids to produce winged offspring thus facilitating future long-distance dispersal away from the predators (Kunert et al., 2005).  Aphid alarm pheromone can also act to help natural enemies find their aphid prey (e.g. Micha & Wyss, 1996), in this case acting as a kairomone.

The use of sex pheromones in integrated pest management is well established (Witzgall et al., 2010) and works very effectively in most cases. More recently, researchers at Rothamsted Research have courted controversy by trialing GM wheat that has been engineered to produce aphid alarm pheromone.  Many entomologists, including me, although finding the concept (Yu et al., 2012) interesting, doubt that it will work in a field situation.  I can certainly see a role for using alarm pheromones as an alternative to conventional chemical control of insect pests and it will be interesting to see if it will prove as effective as using sex pheromones.

 

References

Bowers, W. S., Nault, L. R., Webb, R. E. & Dutky, S. R. (1972). Aphid alarm pheromone: isolation, identification, synthesis. Science 177, 1121-1122.

Busgen, M. (1891)  Der Honigtau. Biologische Studien an Pflanzen und Pflanzenläusen.  Jenaische Zeitschrift für Naturwissenschaft, 25, 339-428

Calam, D.H. & Youdeowei, A. (1968) Identification and functions of secretion from the posterior scent gland of fifth instar larva of the bug Dysdercus intermedius. Journal of Insect Physiology, 14, 1147-1158

Clegg, J.M. & Barlow, C.A. (1982) Escape behaviour of the pea aphid, Acyrthosiphon pisum (Harris) in response to alarm pheromone and vibration. Canadian Journal of Zoology, 60, 2245-2252.

Dahl, M. L. (1971). Über einen Schreckstoft bei Aphiden. Deutsche Entomologische Zeitschrift 18, 121-128.

Dixon, A. F. G. (1958). The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London,110, 319-334.

Dixon, A. F. G. (1958). The protective function of the siphunculi of the nettle aphid, Microlophium evansi (Theob.). Entomologist’s Monthly Magazine, 94, 8.

Edwards, J.S. (1966) Defence by smear: supercooling in the cornicle wax of aphids.  Nature,  211, 73-74.

Hottes, F. C. (1928). Concerning the structure, function, and origin of the cornicles of the family Aphididae. Proceedings of the Biological Society of Washington 41, 71-84.

Kislow, C.J. & Edwards, L.J. (1972)  Repellent odour in aphids.  Nature, 235, 108-109.

Kunert, G., Otto, S., Rose, U.S.R., Gershenzon, J., & Weisser, W.W. (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters, 8, 596-603.

Larsen, K.S. (1988) Responses of different age classes of the rose-grain aphid, Metopolophium dirhodum (Wlk.) to attack by a simulated predator.  Journal of Applied Entomology, 105, 455-459.

Montgomery, M. E. & Nault, L. R. (1977). Comparative response of aphids to the alarm pheromone, (E)-B-farnesene. Entomologia experimentalis et applicata 22, 236-242.

Micha, S.G. & Wyss, U. (1996)  Aphid alarm pheromone (E)-B-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidinae).  Chemoecology, 7, 132-139

Nault, L. R., Montgomery, M. E. & Bowers, W. S. (1976). Ant-aphid associations: role of aphid alarm pheromone. Science 192, 1349-1351.

Nordlund, D. A. & Lewis, W. J. (1976). Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. Journal of Chemical Ecology 2, 211-220.

Strong, F.E. (1966)  Observations on aphid cornicle secretions.  Annals of the Entomological Society of America, 60, 668-673.

Sunderland, K.D., Fraser, A.M., & Dixon, A.F.G. (1986) Field and laboratory studies on money spiders (Linyphiids) as predators of cereal aphids. Journal of Applied Ecology, 23, 433-447.

Wientjens, W. H., Lakwijk, C. J. M., & Van Der Marel, T. (1973). Alarm pheromone of grain aphids. Experientia, 29, 658-660.

Wohlers, P. (1980). Die fluchtreaktion der erbsenlaus Acyrthosiphon pisum Aausgelöst durch alarmpheromon und zusätzliche reize. Entomologia experimentalis et applicata 27, 156-168.

Witzgall, P., Kirsch, P. & Cork, A. (2010) Sex pheromones and their impact on pest management. Journal of Chemical Ecology, 36, 80-100.

Yu, X.D, Pickett, J., Ma, Y.Z., Bruce, T., Napier, J., Jones, H.D. & Xia, L.Q. (2012)  Metabolic engineering of plant-derived (E)-β-farnesene synthase genes for a novel type of aphid-resistant genetically modified crop plants.  Journal of Integrative Plant Biology, 54, 282-299.

 

Post Script

A brief guide to mones

An allomone is any chemical substance produced and released by an individual of one species that affects the behaviour of a member of another species to the benefit of the originator but not the receiver e.g. the ability of some plants to release aphid alarm pheromen and thus deter aphids form landing on them.

An apneumone is any substance produced by nonliving material that benefits a recipient species but is detrimental to a different species associated with the non-living material

A kairomone is a semiochemical, emitted by an organism, which mediates interspecific interactions in a way that benefits an individual of another species which receives it, without benefiting the emitter.  For a detailed critique of the term kairomone see Ruther et al. (2002).

A pheromone is a secreted or excreted chemical factor that triggers a social response in members of the same species. Pheromones are chemicals capable of acting outside the body of the secreting individual to impact the behaviour of the receiving individual e.g. alarm pheromones, food trail pheromones and sex pheromones.

A synomone is a substance produced by an individual of one species that benefits both the producer and the recipient which is of a different species.  An example is the release of chemical elicitors by plants that attract entomophagous insects when they are attacked by herbivores.

 

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