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

Not all aphids grow up to be aphids – the enemy within

It has been said that if aphids had their own way and unlimited resources the world as we know it would be 149 km deep in the cute little beasts (Harrington, 1994 ). Last year I wrote about how predators that feed on aphids, although useful, don’t really cut the mustard when it comes to keeping them in check and suggested that their host plants played a major role in keeping aphids from taking over the World.  While they do play an important part in keeping aphid populations under control, and are aided and abetted by aphid specific predators, there are, however, some much more efficient aphid-specific natural enemies out there.  They may be less conspicuous than the brightly coloured ladybirds that we often see munching their way through aphid colonies; public perception of their name may make people wince, but these beautiful and graceful creatures make sure that our appetite for salads and exotic vegetables out of season is satisfied safely and efficiently.  Their life cycles rival that of their prey, or should that be hosts, and entomologists fondly imagine that the film Alien was inspired by them 😊

I am, of course, talking about parasitic wasps, or parasitoids as they are more commonly known.  They are called parasitoids because unlike true parasites which generally speaking keep their hosts alive, insect victims of these wasps will, if successfully parasitized, die well before their non-parasitized relatives. In case you were wondering, the term parasitoid was coined by the Finnish Hemipterist, Odo Reuter (1913).  Aphids are not the only insects that are attacked by parasitoid wasps. The action of insect parasites has been known about for over two hundred years.  Erasmus Darwin, grandfather of the more famous Charles, noted that Ichneumonid wasps parasitised cabbage white butterfly caterpillars and so should be encouraged by gardeners (Darwin, 1800).  This is not the only early mention of parasitic insects in this context; Wheeler (1928), points out that back in the 1850s, two Italian entomologists, Camillo Rondani and Vittore Ghiliana also suggested the use of parasitic insects as biological control agents.  Aphid pests of glasshouse crops originally controlled mainly by predators (van Lenteren & Woets, 1988) are now routinely controlled by the application of commercially produced Braconid and Chalcid wasps (Boivin et al., 2012; van Lenteren, 2012).

Three commonly used aphid parasitoid biological control agents in action. Images from http://biologicalservices.com.au/products/aphelinus-2.html and https://www6.inra.fr/encyclopedie-pucerons/Especes/Parasitoides/Braconidae-Aphidiinae/Praon-volucre

When people think of Hymenoptera, they tend to think of bees, Vespid wasps and ants as being the most important and abundant.  They are very much mistaken.  The Parastica, or parasitoid wasps, are, by a huge margin, the most speciose and abundant section of

Parasitoids clearly dominate the Hymenopteran fauna of the British Isles (Many thanks to Natalie Dale-Skey of the NHM for permission to use this).

the Hymenoptera both in the UK and elsewhere

In the tropics the parasitoids are even more dominant. Data from Gaston et al., (1996).

Once parasitized, the egg(s), unless they are encapsulated by the aphid ‘immune’ system, hatch and begin to feed on the internal tissues of their, presumably, unsuspecting aphid host.  The parasitoid larvae avoid feeding on vital parts of the aphid, so that it can continue to grow and develop and provide food for the parasitoid, until the parasitoid is ready to pupate. Once the parasitoid is ready to pupate it delivers the coup de grace putting the aphid out of its misery and allowing the formation of the ‘mummy’ in

The three most common types of aphid mummies.  Images from http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers,  http://biologicalservices.com.au/products/aphelinus-2.html and https://farm1.static.flickr.com/327/18532751584_becc0e56e9_b.jpg respectively.

which the parasitoid completes its development before sawing its way out to emerge as a winged adult ready to seek out new hosts, leaving a characteristic neat circular hole in mummy case. In case you were wondering why the mummy of Praon volucre looks like it is sitting on a plate, this because, unlike the other aphid parasitoids, the final instar cuts its way out of the bottom of the aphid and spins its cocoon externally underneath the remnants of the aphid, hence the ‘plate’ (Beirne, 1942).

And out she comes; emerging parasitoid – http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers

 

Lysiphelbus testaceipes  Photo by J.K.Clark, University of California Statewide IPM Project

Once an aphid, now a hollow mummy; note the neat emergence holes.  Aphid parasitoids are very much tidier than the parasitic lifeform in the classic film Alien 🙂

Another aspect of their life style that makes parasitoids a breed apart from true parasites, is that as well as using aphids as egg laying sites for their larvae, the adults like to snack on them every now and then to help mature more eggs and to keep up their energy levels; sometimes quaintly described as predatism (Flanders, 1953).  Although the parasitoids can make feeding attacks at any time, they appear to feed first and then start laying their eggs (e.g. Collins et al., 1981).

Parasitoids are widely used as biological control agents in glasshouses and other protected environments as they are generally regarded as being more effective than predators (Debach & Rosen, 1991), although there is some support that generalist predators can play a significant part in biological control in the wider environment (Symondson et al., 2002; Gontijo et al., 2015).  That said, aphid parasitoids seem to be fairly host specific in that commercial companies offer specific parasitoid mixtures to control different aphid pest species e.g.  https://www.koppert.com/pests/aphids/product-against/aphipar/ [Note this is NOT an endorsement]. In fact it has been suggested that the relationship between aphids and their parasitoids can be used to clarify aphid taxonomic relationships (Mackauer, 1965). On the other hand, there are very few examples of monophagous aphid parasitoids, most being described as oligophagous (Stary & Rejmanek, 1981).   So given that there is a fair bit of evidence that the parasitoids attacking aphids do show some discrimination in their choice of hosts, how do they find them?

Parasitoids in general were originally thought to be “possessed of an unerring instinct that guided them in their search for hosts” but Cushman (1926) rebutted this idea pointing out that actually the parasitoids first home in on the habitat or food plant that their host lives in and then search for their host (Laing, 1937).   The parasitoids referred to by Cushman and Laing, are however, not parasitoids of aphids, attacking lepidopteran leaf miners and carrion feeding flies respectively, so you might perhaps think that aphid parasitoids could have a different strategy. Although habitat selection by parasitoids of lepidopteran larvae (Thorpe & Caudle, 1938) and sawfly larvae (Monteith, 1955), using olfactory cues of their host’s food plant was confirmed readily easily and early on, the situation with aphids was less clear cut. Manfred Mackauer for example, suggested that aphid parasitoids might be using visual cues, such as leaf deformities or damage to find their aphids hosts (Mackauer, 1965).  The breakthrough came when three cabbage loving entomologists from the USA used an olfactometer to first show that the Braconid parasitoid Diaeretiella rapae, responded positively to the odour of collards (what we in the UK call spring greens) and second to show a very strong preference for them to lay their eggs in the aphid Myzus persicae when it was feeding on crucifers rather than other host plants.  They attributed this to the presence of mustard oil, the chemical that gives cabbages their distinctive taste and suggested that once the aphid host plant was found then the parasitoids used visual cues to find their aphid victims (Read et al., 1970).  Six years later it was firmly established that parasitoids in general used olfactory cues both to locate the habitat of their host (long-range) and then a short-range to find and confirm the identity (contact chemicals) their insect hosts (Vinson, 1976).

It was thought that the aphid parasitoids were chemically ‘conditioned’ during their larval life within the aphid feeding on a host plant and that this influenced their adult host preferences (e.g. Sheehan & Shelton, 1989; Wickremasinghe & Van Emden, 1992).  These, and other similar results, seemed to support the Hopkins host selection principle (Hopkins, 1917) which states that adult preferences are learnt as larvae.  A very neat experiment by van Emden et al., (1996) proved this hypothesis wrong. They transferred aphid mummies from the plant on which they had been parasitized on to another host plant and this changed the preference of the emerging adult, seeming to suggest that this was how aphid parasitoids developed their host preferences.  Now comes the neat, and very tricky part; if however, the parasitoid pupae were removed (very carefully) from the mummy case and reared to adulthood in the absence of a host plant or mummy and kept in a glass tube, the emerging adults showed no preference for particular host plants, clearly showing that adult preferences were  not determined during larval development but ‘conditioned’ by exposure to the external skin of the aphid mummy on emergence (van Emden et al., 1996).  Using aphids reared on an artificial diet (Douloumpaka & van Emden, 2003) showed that the it was very likely that the mother parasitoid leaves a chemical cue in or around the egg(s) she lays and that this is later incorporated into the silk of the parasitoid pupa, thus inducing the host preference seen as an adult.

An additional twist to the story is that male and female parasitoids differ in their responses to odours.  Both sexes of Aphidius uzbekistanicus and A. ervi, parasitoids of cereal aphids in the UK, respond to plant odours, but only females respond to aphids (Powell & Zhi-Li, 1983).  Males of both species are, however, attracted to the odours of their respective females, suggesting the existence of a sex pheromone. The existence of a sex pheromone in aphid parasitoids had been suggested a few years earlier when it was shown that male D. rapae attempted to copulate with filter paper that had had female abdomens crushed on them (Askari & Alisha, 1979).  The existence of sex pheromones in aphid parasitoids has now been shown in several species (e.g. Decker et al., 1993; McNeil & Broduer, 1995).  Strangely, female parasitoids also respond to sex pheromones, but in their case, the sex pheromones of aphids.  It turns out that they ‘parasitise’ aphids in more than one way, they home in on their prey using the aphid sex pheromone and this enables them to find a suitable overwintering host (Hardie et al., 1991).  At other times of the year they also use other aphid indicators; several studies have shown that parasitoids use the presence of aphid honeydew to help them find their hosts (Budenberg, 1990; Bouchard & Cloutier, 1984; Gardner & Dixon, 1985).

Predators of aphids such as ladybirds use chemical markers to warn other ladybirds that they have laid eggs near aphid colonies, thus reducing the chances of cannibalism and competition (e.g. Oliver et al., 2006). Given that the eggs of aphid parasitoids are laid internally, they are in effect invisible, it would make sense if the parasitoids ‘marked’ their hosts in some way to avoid other parasitoids laying their eggs in an already parasitized aphid, superparasitism.  Sure enough, there is some evidence that some adult parasitoids can recognise aphids that already have larval parasitoids developing inside them although they don’t seem to be able to consistently recognise already parasitized aphids until some hours afterward (e.g. Cloutier et al., 1984).  In some cases, it seems that it is the aphid herself that prevents superparasitism by reacting more aggressively towards parasitoids after being attacked once (Gardner & Dixon, 1984) and also by the presence of dried siphuncular secretions on the aphid’s skin (Outreman et al., 2001).  The waxy secretion had an effect for up to a day or so after which the internal changes caused by the developing parasitoid larvae were enough to deter further oviposition attempts.

It is a good thing for the poor aphids that they have such a high reproductive rate, or they would truly be in dire straits.  On the other hand, as exemplified by the words of Jonathan Swift (1733),

“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em,
And so proceed ad infinitum”

there are parasites of parasitoids, the hyperparasites, that help keep the numbers of parasitoids under control, and thus, indirectly, help aphids remain relatively abundant.

 

References

Askari, A. & Alisha, A. (1979) Courtship behavior and evidence for a sex pheromone in Diaeretiella rapae (Hymenoptera: Braconidae), the cabbage aphid primary parasitoid. Annals of the Entomological Society of America, 72, 79-750.

Beirne, B.P. (1942) Observations on the life-history of Praon volucre Haliday (Hym.: Braconidae), a parasite of the mealy plum aphis (Hyalopterus arundinis Fab.). Proceedings of the Royal Entomological Society of London, Series A, General Entomology, 17, 42-47.

Boivin, G., Hance, T. & Brodeur, J. (2012) Aphid parasitoids in biological control.  Canadian Journal of Plant Science, 92, 1-12.

Bouchard, Y. & Cloutier, C. (1984) Honeydew as a source of host-searching kairomones for the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae).  Canadian Journal of Zoology, 62, 1513-1520.

Budenberg, W.J. (1990) Honeydew as a contact kairomone for aphid parasitoids.  Entomologia experimentalis et applicata, 55, 139-148.

Cloutier, C., Dohse, L.A. & Bauduin, F. (1984) Host discrimination in the aphid parasitoid Aphidius nigripes. Canadian Journal of Zoology, 62, 1367-1372.

Collins, M.D., Ward, S.A., & Dixon, A.F.G. (1981) Handling time and the functional response of Aphelinus thomsoni, a predator and parasite of the. Journal of Animal Ecology, 50, 479-487.

Cushman, R.A. (1926) Location of individual hosts versus systematic relation of hots species as a determining factor in parasitic attack. Proceedings of the Entomological Society of Washington, 28, 5-6.

Darwin, E. (1800) Phytologia: or The Philosophy of Agriculture and Gardening. P. Byrne, Grafton Street, London.

Debach, P. & Rosen, D. (1991) Biological Control by Natural Enemies, Cambridge University Press, New York.

Decker, U.M., Powell, W. & Clark, S.J. (1993) Sex pheromone in the cereal aphid parasitoids Praon volucre and Aphidius rhopalosiphi.  Entomologia experimentalis et applicata, 69, 33-39.

Douloumpaka, S. & van Emden, H.F. (2003) A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Mysuze persicae Sulzer.  Physiological Entomology, 28, 108-113.

Flanders, S.E. (1953) Predation by the adult Hymenopteran parasite and its role in biological control. Journal of Economic Entomology, 46, 541-544.

Gardner, S.M. & Dixon, A.F.G. (1984) Limitation of superparasitism by Aphidius rhopalosiphi: a consequence of aphid defensive behaviour. Ecological Entomology, 9, 149-155.

Gardner, S.M & Dixon, A.F.G. (1985) Plant structure and foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae).  Ecological Entomology, 10, 171-179.

Gaston, K.J., Gauld, I.D. & Hanson, P. (1996) The size and composition of the hymenopteran fauna of Costa Rica.  Journal of Biogeography, 23, 105-113.

Griffiths, D.C. (1960) The behaviour and specificity of Monoctonus paldum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigbi (Mosley) on lettuce. Bulletin of Entomological Research, 51, 303-319.

Hardie, J., Nottingham, S.F., Powell, W. & Wadhams, L.J. (1991) Synthetic aphid sex pheromone lures female parasitoids.  Entomologia experimentalis et applciata, 61, 97-99.

Harrington, R. (1994) Aphid layer. Antenna, 18, 50-51.

Hopkins, A.D. (1917) Contribution to discussion.  Journal of Economic Entomology, 10, 92-93.

Holler, C. (1991) Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments and sex pheromone specificities (Hymenoptera, Braconidae, Aphidiinae. Systematic Entomology, 16, 15-28.

http://www.biologicalcontrol.info/aphid-primary-and-hyperparasitoids.html

Laing, J. (1937) Host-finding byinsect parasites 1. Observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescens.  Journal of Animal Ecology, 6, 298-317.

Mackauer, M. (1965) Parasitological data as an aid in aphid classification. Canadian Entomologist, 97, 1016-1024.

McNeil, J.N. & Brodeur, J. (1995) Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripes.  Journal of Chemical Ecology, 21, 959-972.

Monteith, L.G. (1955) Host preferences of Drino bohemica Mesn. (Diptera; Tachnidae) with particular reference to olfactory responses.  Canadian Entomologist, 87, 509-530.

Oliver, T.H., Timms, J.E.L., Taylor, A. & Leather, S.R. (2006) Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks. Bulletin of Entomological Research, 96, 25-34.

Outreman, Y., Le Ralec, A., Plantegenest, M., Chaubet, B, & Pierre, J.S. (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology, 47, 339-348.

Powell, W. & Zhi-Li, Z. (1983) The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants.  Physiological Entomology, 8, 439-443.

Reuter, O.M. (1913). Lebensgewohnheiten und Instinkte der Insekten (Berlin: Friendlander).

Stary, P. & Rejmanek, M. (1981) Number of parasitoids per host in different systematic groups of aphids: The implications for introduction strategy in biological control (Homoptera: Aphidoidea; Hymenoptera: Aphidiidae). Entomologica Scandinavica, Suppl. 15, 341-351.

Riley, W.A. (1931) Erasmus Darwin and the biologic* control of insects. Science, 73, 475-476.

Sheehan, W. & Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae).  Journal of Insect Behavior, 2, 743-759.

Symondson, W.O.C., Sunderland, K.D., & Greenstone, M.H. (2002) Can generalist predators be effective bicontrol agents? Annual Review of Entomology, 47, 561-594.

Thompson, W.R. (1930) The principles of biological control. Annals of Applied Biology, 17, 306-338.

Thorpe, W.H. & Caudle, H.B. (1938) A study of the olfactory responses of insect parasites to the food plant of their host.  Parasitology, 30, 523-528.

Van Emden, H.F., Spongal, B., Wagner, E., Baker, T., Ganguly, S. & Douloumpaka, S. (1996) Hopkins’ ‘host selection principle’, another nail in its coffin.  Physiological Entomology, 21, 325-328.

Van Lenteren, J.C. (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57, 1-20.

Van Lenteren, J.C. & Woets, J. (1988) Biological and integrated control in greenhouses.  Annual Review of Entomology, 33, 239-269.

Vinson, S.B. (1976) Host selection by insect parasitoids.  Annual Review of Entomology, 21, 109-133.

Wheeler, W.M. (1922). Social life among the insects: Lecture II. Wasps solitary and social. Scientific Monthly, 15, 68-88.

Wheeler, W.M. (1928) Foibles of Insects and Men.  Alfred Knopf, New York

Wickremasinghe, M.G.V. & Van Emden, H.F. (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology, 17, 207-304.

*This is how he spelt it; not a mistake on my part J

Prunella – mistress of plasticity

Now that I have your attention, this is not an article about soft porn or fetishes, but rather a paean for that humble ‘weed’ Prunella vulgaris – Self-heal, Heal all, Woundwort, Heart of the Earth and many other names, depending on where in the World you come from.   Prunella vulgaris is in the family Lamiaceae, so related to mints and dead-nettles.  It is an edible weed, the young leaves can be used in salads and it can also be used in soups, stews, or used whole and boiled as a pot herb.

The instantly (to me at any rate) recognisable flower of Prunella vulgaris

Prunella as I will now familiarly call her, has a very wide geographical native range and has also been introduced into South America where she does very well indeed (Godoy et al., 2011).

Distribution of Prunella vulgaris, blue native, brown introduced. http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:455176-1

 The name Prunella is derived from ‘Brunella’, a word which is itself a derivative, coming from the German name for quinsy, (a type of throat inflammation), die Braüne, which it was historically used to cure.  That is the other aspect of this glorious plant, it has many medicinal properties, hence the many common names refer to its healing powers, almost as many as Athelas of Lord of the Rings fame 😊  It was traditionally used in European herbal medicine for sore throats, fever reduction and like Athelas, for accelerating the healing of wounds (Matthiolus, 1626).  More recently it has become of interest as a possible cure for conditions associated with the herpes simplex virus (Psotováa et al., 2003) and inhibiting anaphylactic shock and other immediate type allergic reactions (Shin et al., 2001).  So truly a wonder drug, and again proving that “Old Wives Tales” are in many cases based on more than just superstition.

My interest in Prunella vulgaris, is however, based on its wondrous plasticity, as the three photographs below show nicely.  Depending on grazing (or mowing) pressure, Prunella can grow to reproductive maturity at heights  ranging from just over 2 cm to just under 30 cm. Truly remarkable.

I am of course, not the first person to be fascinated by this plasticity and the taxonomic and evolutionary ins and outs of this lovely plant (Nelson, 1965; Warwick & Briggs, 1979) but I still find it fascinating, and who knows, perhaps one day I might do some work on it myself 😊

The other thing that I like about Prunella is that she is also provides a living for aphids.  She has her own rare and specific one, Aphis brunellae, but is also kind enough to let a few other species make a living on her, Aphis gossypii, Aphis nasturtii, Aulacorthum solani,  Macrosiphum euphorbiae, the ubiquitous Myzus persicae, M. ornatus and Ovatomyzus chamaedrys (Blackman & Eastop, 2006).

Aphis brunellae, rare in the UK – with thanks to the two Bobs for permission to use the photograph. http://influentialpoints.com/Images/Aphis_brunellae_colony_on_Prunella_vulgaris_c2015-08-21_15-37-27ew.jpg

 

Finally, you will have noticed that the Prunella aphid is A. brunellae, which is derived from the original name of Prunella (I guess Prunella Scales is happy, she could have been Brunella Scales).  Interestingly, her alter-ego was not removed until fairly recently, her tombstone is shown below.

References

Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World’s Herbaceous Plants and Shrubs Volume 1 Host Lists and Keys.  Wiley, Oxford.

Godoy, O., Saldaña, A., Fuentes, N., Valladares, F. & Gianoli, E. (2011)  Forests are not immune to plant invasions: phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biological Invasions, 13, 1615-1625.

Matthiolus, P.A. (1626) Kräuterbuch.  Noringberg.

Nelson, A.P. (1965) Taxonomic and evolutionary implications of lawn races in Prunella vulgaris (Labiatae). Brittonia, 17, 160-174.

Psotová, J., Kolá, M., Sousek, J., Ívagera, Z., Vicar, J. &Ulrichová, J. (2003) Biological activities of Prunella vulgaris extract. Phytotherapy Research, 17, 1082-1087.

Shin, T.Y., Kim, Y.K. & Kim, H.M. (2001) inhibition of immediate-type allergic reactions by Prunella vulgaris in a murine model.  Immunopharmacology & Immunotoxicology, 23, 423–435.

Warwick, S.I. & Briggs, D. (1979) The genecology of lawn weeds III. Cultivation experiments with Achillea millefolium L., Bellis perennis L., Plantago lanceolata L., Plantago major L. and Prunella vulgaris L. collected from lawns and contrasting grassland habitats.  New Phytologist, 83, 509-536.

 

Do pea aphids rule the world? Joint UK-French Aphid Meeting Paris

Last week (5^th to 6^th November 2015) I had the great privilege and pleasure to attend an aphid conference in Paris – my favourite insects and my favourite city – heaven!  The conference was mainly organised by our French colleagues from INRA, under the direction of Jean-Christophe Simon with help from Richard Harrington, recently retired from Rothamsted Research, and a tiny bit of input from me.

The meeting was held at the Societe Nationale D’Horticulture De France, a building cunningly hidden away down a long passageway off the Rue de Grenelle which debuts into a small courtyard where I found the main entrance and was reassured by the sight of the

organisers feverishly getting name tags ready (I was very early as had thought it would take longer to walk there than it actually did) and

a suitably amusingly appropriate sign on the door.

I was greeted enthusiastically by Jean-Christophe, caused a bit of a hiatus by having to have my name badge located and was then pointed gently, but firmly at the coffee 🙂

The rest of the delegates began to arrive some twenty minutes later or so and shortly after we were ushered into the lecture theatre, which was very full.

After getting over the shock of being told that there was no Wifi available (that put paid to my plans for Tweeting), I settled down to enjoy the morning. The conference began with an invited presentation from Takema Fukatsu from Japan who gave us an overview on symbiosis, evolution and biodiversity.   This was then followed by two shorter talks of 12.5 minutes each leading us into the first coffee break.  One of the great things about this conference was, that apart from the plenary presentation, all talks were restricted to 10 minutes with 2.5 minutes for questions.  This meant that we got to hear 40 (yes forty) talks over the two days and that we had refreshment breaks every 75 minutes, (the coffee was excellent).  The refreshment breaks were half an hour long, and lunch was an hour, thus giving delegates plenty of time to mix and chat about their work.

There were just over a 100 delegates coming from eight different countries, although as one might expect, most were from France and the UK. It was great to see so many people working on aphids, although not all could be described as “aphidologists” sensu stricto, but I am sure that everyone there would be happy to be included under that description as sensu lato 🙂 Sadly in the UK the number of aphidologists has declined greatly since I was a student, especially those working on their ecology and morphotaxonomy.

The focus of the talks and posters, of which there were 21, was predominantly on the interactions of aphids with their host plants and natural enemies. The role of symbionts in these interactions and the molecular mechanisms involved was especially highlighted, in particular those involved with the pea aphid, Acyrthosiphon pisum.  Aproximately 40% of the talks were on the pea aphid, and a further 28% on the most pestiferous aphid in the world, Myzus persicae and its ability to develop resistance to pesticides.  Although I find aphid symbionts fascinating, I am a bit concerned that they and the pea aphid seem to be taking over the world!  Given the number of talks, I am not going to review them all.   For those interested the full programme and abstracts can be found here.  Highlights for me were Christoph Vorburger from ETH who gave an entertaining talk about the effect that endosymbionts have in protecting aphids against parasitoids, and making me feel old, Ailsa McLean from Oxford University, whom I first met when she was in her pram (she is the daughter of Ian Mclean with whom I shared a lab when we were PhD students).  I was also very pleased to be chairing the session in which Charles Dedryver (now retired) was speaking about the history of aphidology.  I was less happy that I had to cut his talk short, but my duties left me no other choice 🙂  Despite Charles and I exchanging reprints for almost 40 years, this was the first time that we had ever come face to face.

All in all a fantastic conference and many congratulations to the team from INRA for organising it so well. My one concern, which I touched upon earlier was the predominance of the pea aphid as a model organism and the overriding focus on the molecular aspects of the various interactions.  I find it a little worrying that I can find statements in papers such as “This is an exciting time for pea aphid biologists”  (Brisson, 2010), which hardly indicates a broad viewpoint. As a further indication of an overly narrow focus, during the breaks it was noticeable that of the people who ventured outside, I was the only one turning leaves over and looking for aphids, the others were indulging their nicotine habits.

It is important that as aphidologists, entomologists and ecologists we do not lose sight of the big picture.

 

Reference

Brisson, J.A. (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philosophical Transactions of the Royal Society B, 365, 60-616

 

Sensu stricto in the narrow sense; Sensu lato broadly speaking

 

A non-entomological post script

The added bonus of having the conference in Paris was that my wife had an excuse to pop over for the weekend and I was able to extend my visit. The weather was fantastic and we had a great time eating, drinking and seeing as many sights as we could fit in.  Luckily the weather was glorious.

My favourite sort of pudding – Café Gourmand (at Le Café Gourmand)

We rode the funicular to the top of Montmartre, something which despite having visited Paris at least once a year for the last 15 years or so, we had never done. Then after visiting the Montmartre Museum, we walked down to the cemetery.  Paris has some great cemeteries and we never miss the chance to see what curiosities we can find.

A psychoanalyst with a macabre sense of humour Dr. Guy Pitchal (1922-1989), Psychoanalyst known for working with many French celebrities — including the singer Dalida, who is buried nearby.

The Great Nijinsky – looking a bit fed-up?

Emile Zola – we came across his magnificent tomb entirely by accident, after taking a wrong flight of stairs.

Cancan dancer extraordinaire, La Goulue (The Glutton).

Robert Mayet – Inventor of the moped

Looking for somewhere to eat on Saturday evening we came across a number of shops already preparing for Christmas.

Christmas will apparently soon be with us!

Bees get everywhere – no idea what this was about but saw it as we were heading for the Eurostar.

 

Entomological classics – The Moericke (Yellow) Pan Trap

Most, if not all field entomologists, will have used Yellow pan traps and been delighted in a horrified sort of way, by the huge number of usually small and hard to identify insects that they attract.

Moericke (Yellow) Pan trap in use in the tropics.  http://oilpalmbiodiversity.com/news-update-2/

Moericke (Yellow) Pan trap in use in the far north.   http://thebuggeek.com/2010/07/20/my-life-in-the-north-so-far-the-halfway-point/yellow-pan-and-gear/  Many thanks to Crystal Ernst for permission to use this picture.

They are of course, designed to do just that and so as entomologists we should be happy that they are so good at their job.  The secret of their success lies in their colour, yellow, which is highly attractive to many flying insects, flies (Disney et al., 1982) and aphids (Eastop, 1955) being particularly attracted to them as are bees and wasps (Vrdoljak & Samways, 2012; Heneberg & Bogusch, 2014).  They are also attractive to thrips (Thysanoptera) (Kirk, 1984) and have long been the subject of many comparative studies (e.g. Heathcote, 1957), although the prize for one of the most elaborate and labour intensive studies involving pan traps must go to my friend and former colleague Thomas Döring (Döring et al., 2009) who ran an experiment using pan traps of seventy, yes seventy, different colours!  They are easy to deploy and range from expensively bought made-to-order versions to yellow plastic picnic plates, yellow washing up basins and even Petri dishes painted yellow.  They can be mounted on poles and sticks or just placed on the ground; to say that they are versatile is a bit of an understatement.

So who invented the pan trap?  I have of course given the name of the inventor away in the title of this article. They were invented surprisingly relatively recently, by the German entomologist Volker Moericke (Moericke, 1951), although I suspect that he used them some years before the publication of the paper.  These first pan or Moericke traps as we should call them, were made of tin, painted yellow, and mounted on three wooden sticks.  They were 22 cm in diameter and 6 cm deep and filled with a mixture of water and formaldehyde .  Moericke was working on the aphid Myzus persicae .  He was particularly interested in aphid vision and host location (Moericke, 1950). He observed that the aphids were able to distinguish between the red-yellow-green end of the spectrum and the blue-violet end.   This then stimulated him to try trapping aphids using coloured pan traps (Moericke, 1951).  He observed that the aphids were attracted to the yellow pan traps and behaved as if over a host plant resulting in them landing in the liquid from which they were unable to escape.  Although he noted that the traps were extremely effective at catching aphids he did not comment on what other insects he found in the traps.

The first Moericke (yellow) Pan trap (from Moericke, 1951).

This simple, yet effective design has now become an essential part of the entomologist’s tool kit being used by field entomologists of every ilk working  across the world in every habitat.  They are truly an influential invention and worth of being named an entomological classic.  Given the wide usage of these traps and their remarkable efficacy I think that we should make every effort to acknowledge their inventor by calling their modern plastic counterparts Moericke Traps.

 

References

Disney, R.H.L., Erzinçlioglu, Y.Z., Henshaw, D.D.C., Howse, D., Unwin, D.M., Withers, P. & Woods, A. (1982) Collecting methods and the adequacy of attempted fauna surveys with reference to the Diptera.  Field Studies, 5, 607-621.

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

Eastop, V.F. (1955)  Selection of aphid species by different kinds of insect traps.  Nature, 176, 936

Heathcote, G.D. (1957) The comparison of yellow cylindrical, flat and water traps, and of Johnson suction traps for sampling aphids.  Annals of Applied Biology, 45, 133-139.

Heneberg, P. & Bogusch, P. (2014)  To enrich or not to enrich?  Are there any benefits of using multiple colors of pan traps when sampling aculeate Hymenoptera?  Journal of Insect Conservation, 18, 1123-1136

Kirk, W.D.J. (1984)  Ecologically selective traps.  Ecological Entomology, 9, 35-41

Moericke, V. (1950)  Über das Farbsehen der Pfirsichblattlaus (Myzodes persicae Sulz.).  Zeitschrift für Tierpsychologie, 7, 265-274.

Moericke, V. (1951)  Eine Farbafalle zur Kontrolle des Fluges von Blattlausen, insbesondere der Pfirsichblattlaus, Myzodes persicae (Sulz.).  Nachrichtenblatt des Deutschen Pflanzenschutzdiensten, 3, 23-24.

Vrdoljak, S.M. & Samways, M.J. (2012)  Optimising coloured pan traps to survey flower visiting insects.  Journal of Insect Conservation, 16, 345-354

 

Post script

Many thanks to those readers who supplied me with Moericke’s first name, which in the original version of this post was lacking.

 

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 -42^oC (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.

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 -26^oC 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 -10^oC 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.

 

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.

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 -20^oC, 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.

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