Category Archives: Aphids

Booze, sweat and blood – the birth of a paper

Of my top five most cited papers two are reviews, two are opinion pieces and one is a ‘real’ paper.  I have written about the serendipitous event that resulted in my second most cited paper (Leather, 1988), but now it is the turn for Number 5 to make the headlines 🙂 Number 5 (Ward et al., 1998), is a ‘real’ paper in that it tests an hypothesis and is based on data. It would, however, almost certainly never have come into existence if my friend and former lab mate, Seamus Ward, hadn’t come to visit me at Silwood Park in the spring of 1997.

Seamus was in the year below me in Tony Dixon’s lab, originally taken on to work on the maple aphid, but it transpired that his life history traits were not suited to maintaining host plants and aphid cultures.  Luckily it turned out that his true talents were in the area of theory and mathematical ecology; when you were talking to him about your aphids and what they were doing Seamus would sit there turning your description into equations. He thus ended up doing a PhD looking at life-history traits in aphids.  I make no claims to being mathematically oriented, but do take a quiet pride in being pretty good at running practical experiments and this made for a good partnership in the group, in that Seamus would come to me when he needed some experimental support (real data). This was mutually beneficial and resulted in papers we would not necessarily have written otherwise (Leather et al., 1983; Ward et al., 1984).

Having not seen Seamus for some time, since finishing his post-doc in the mid-1980s, he had been based in Australia at the University of La Trobe, we were reminiscing about old times. I happened to mention that I had fairly recently examined one of Tony Dixon’s PhD students who had been working on the carrot-willow aphid, Cavariella aegopdii and the evolution of aphid life-cycles (e.g. Kundu & Dixon, 1993, 1995). This of course got us on to talking about host alternation and why, if it is so risky, (there were estimates of less than 1% surviving the journeys between hosts (Taylor, 1977)), some aphid species. albeit only 10%, had adopted that strategy. In another paper, Tony and Raj had suggested that even if only 1 in 10 000 survived

The words that inspired us  – from Dixon & Kundu, 1994)

the migration from host to host, the high fecundities that host alternating aphids can achieve on their primary hosts (Leather & Dixon, 1981), would make it worthwhile (Dixon & Kundu, 1994). This got us thinking – how many aphids did actually make it and could we work it out?  We discussed this for a while over a beer, (we were in the Silwood Bar at the time), and Seamus decided that what we needed were some data of numbers of aphids on the ground and the number of aphids in the air at the same time. As it happened, I had a ten-year run of bird cherry aphid data on their primary host, Prunus padus trees in Roslin Glen (Scotland) (from my bird cherry aphid side project) and as a subscriber to the Rothamsted Aphid Bulletins, I had in my office, copies of the weekly aphid bulletins for the nearest suction trap to Roslin Glen, East Craigs.  This was enough for us to get started.

The bird cherry aphid side project data – still with me today and more analysis yet to be done 🙂

An example of the old paper version of the weekly aphid bulletin – I now subscribe electronically – a great resource https://insectsurvey.com/aphid-bulletin “The Rothamsted Insect Survey, a National Capability, is funded by the Biotechnology and Biological Sciences Research Council under the Core Capability Grant BBS/E/C/000J0200.”

The next day I started collating the field data and Seamus started to model.  We were totally engrossed and kept at it all day, breaking only for meals and coffee. After dinner, armed with a bottle of whisky and bubbling with ideas we returned to the computer and Seamus started taking me through his model and fitting the data.  Following the intricacies of the model was not easy for me and made my brain work so hard that my forehead started to sweat 🙂 Sometime near midnight, the bottle of whisky was empty, we had a working model and could put a figure on how many migrating aphids made it from the secondary host to the primary host – 0.6%.  Now, all we needed to do was to get the official aphid and weather data from the East Craigs suction trap and write the paper, which with the collaboration of Richard Harrington and Jon Pickup of Rothamsted Research Station and East Craigs respectively, we successfully did, the paper being submitted in August 1997, and appearing in early 1998 (Ward et al., 1998). In case you were wondering how many bird cherry aphids make it from the secondary host back to the primary host, for every 1000 that take-off, 6 make it, so less than Roy Taylor’s estimate but more than the number that Raj and Tony suggested were needed to make host alternation viable.

So that is the booze and the sweat accounted for, but what about the blood? I had, as an undergraduate, become a regular blood donor and the day after our marathon data crunch, was my scheduled blood donation.  That sunny morning, and somewhat hung-over, I walked across to the blood wagon, conveniently parked outside my office, made my donation and after my biscuit and cup of tea, headed back to my office.  As I was passing the toilets, I felt the need for a pee, so nipped in to relieve myself, stood at the communal urinals, unzipped and started to pass water, as I did so, my blood pressure dipped and I started to faint, my last thought before I passed out was that I didn’t want to fall face down in the urinal gutter, so pushed away from the wall with one hand. 

Not the actual urinal (they have long since been replaced) but this gives you the idea of what I didn’t want to fall into. Image source

I woke up some time later on the floor bleeding copiously from a head wound caused by me falling across one of the wash basins.  To cut a long story short, I was rushed to the local hospital, my head repaired, and, as I had a post-donation faint, no longer allowed to donate blood.  On the plus side, the paper has been very successful and I have an amusing after-dinner story to tell and the scar to prove it 🙂

References

Dixon, A.F.G. & Kundu, R. (1994) Ecology of host alternation in aphids. European Journal of Entomology, 91, 63-70.

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

Kundu, R. & Dixon, A.F.G. (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology, 64, 245-255.

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.

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

Leather, S.R., Ward, S.A. & Dixon, A.F.G. (1983) The effect of nutrient stress on life history parameters of the black bean aphid, Aphis fabae Scop. Oecologia, 57, 156-157.

Taylor, L.R. (1977) Migration and the spatial dynamics of an aphid, Myzus persicae. Journal of Animal Ecology, 46, 411-423.

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

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.

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Not just sailor aphids, but an aphid ship too – Insect Class Gunboats

Some of you may have come across Reaktion Books and their Animal series, which as well having the usual vertebrate suspects has a refreshingly large number of invertebrate titles, for example, Moth, Ant, Mosquito just to name those gracing my shelves. I had, at one time, the ambition of adding to the collection with Aphid :-). Unfortunately, one of the requirements for inclusion in the series is what one might call a cultural dimension, and despite being fabulously awesome, aphids have not, as yet, made a huge impact on human culture.  In spite of assiduous searching on my behalf, I have not, as yet*, managed to find many instances of aphids making it into the wider human consciousness beyond their undeserved (in my opinion) reputation as mega-pests.

My count to date is a post card, a children’s book, a postage stamp, a sculpture and two poems. Sadly, I don’t feel I can count coloured plates from entomological texts, no matter how beautiful 😦

Punk aphid postcard – adapted from the cover of an issue of New Scientist published in 1977, when our PhD group at the University of East Anglia had our fifteen minutes of fame 🙂

To my knowledge, the only children’s book (or any work of fiction for that matter), with an aphid as the main character.

The World’s classiest stamp – thank you Slovenia for recognising the importance of aphids 🙂

An artist who appreciates the beauty of aphids – Aphid on rose – Beth Biggs.

Of the two poems that mention aphids, Charles Goodrich’s is, in my opinion, the winner, so I have reproduced it in full. I am much less enamoured of Greenfly from Giles Goodland’s collection celebrating insects, The Masses, so have not shared it with you.

A Lecture on Aphids by Charles Goodrich

She plucks my sleeve.
“Young man,” she says, “you need to spray.
You have aphids on your roses.”

In a dark serge coat and a pill box hat
by god it’s my third grade Sunday school teacher,
shrunken but still stern, the town’s
most successful corporate attorney’s mother.
She doesn’t remember me. I holster
my secateurs, smile publicly,
and reply, “Ma’am,

did you know a female aphid is born
carrying fertile eggs? Come look.
There may be five or six generations
cheek by jowl on this “Peace” bud.
Don’t they remind you
of refugees
crowding the deck of a tramp steamer?
Look through my hand lens-
they’re translucent. You can see their dark innards
like kidneys in aspic.

Yes, ma’am, they are full-time inebriates,
and unashamed of their nakedness.
But isn’t there something wild and uplifting
about their complete indifference to the human prospect?”

And then I do something wicked. “Ma’am,” I say,
“I love aphids!” And I squeeze
a few dozen from the nearest bud
and eat them.

After the old woman scuttles away
I feel ill
and sit down to consider
what comes next. You see,
aphids
aren’t sweet
as I had always imagined.
Even though rose wine is their only food,
aphids
are bitter.


“But what about the ship?” I hear you cry.  To cut a long story short, I was looking for images of Aphis species for a lecture, when up popped a picture of a ship, HMS Aphis. I of course immediately jumped down the internet rabbit hole in pursuit and found to

HMS Aphis https://commons.wikimedia.org/wiki/File:HMS_Aphis_AWM_302297.jpeg

my delight that during the first World War, the Admiralty commissioned a class of ships, the Insect Gunboats, for the Royal Navy designed for use in shallow rivers or inshore. Twelve of these were commissioned between 1915 and 1916. They were, in alphabetical order, not in order of commission, Aphis, Bee, Cicala, Cockchafer, Cricket, Glowworm, Gnat, Ladybird, Mantis, Moth, Scarab, and surprisingly, given the huge number of candidates to choose from, a non-insect, Tarantula.

I haven’t been able to discover why someone decided to call them the Insect class or why they choose the names they did.  Most

HMS Aphis, ship’s badges – very pleased to see the siphunculi, somebody did their research.

of them are not particularly pugnacious species with the possible exceptions of the Bee, Gnat, Ladybird, Mantis and the non-insect Tarantula.

Not sure which species of ladybird this is supposed to represent but felt that as an insect often associated with aphids it deserved a mention 🙂

Lepidoptera, Hymenoptera and Diptera

HMS Glowworm – a shame that this is symbolic rather than the actual insect 😦

Sadly, none of the Insect gunboats have survived, HMS Aphis was scrapped in 1947, in Singapore of all places, and the last one, HMS Cockchafer, was sold for scrap in 1949.

Pleased as I was to discover HMS Aphis, I am still a long way off having enough cultural references to convince Reaktion Books that Aphid is a possible title in the series. The Secret Life of Aphids, is however, a real possibility :-).  Finally, if you were puzzled about the sailor aphids I mention in the title, you can satisfy your curiosity by clicking on this link.

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Spore shedding aphids

If you were in the European silkworm business two or three hundred years ago the last thing you wanted to find in your colony were stiff dead caterpillars. Worse still would be if when you picked them up and bent them, they snapped in half and revealed a solid white or green interior, giving them the appearance of a stick of chalk. Horror stricken you realise that your beloved silkworms have been struck down by white or green muscardine disease, or if you were an Italian, calcino; in both cases the name refers to the chalk like appearance of the inside of the stricken larvae.  By the middle of the 19th century the combined effects of the industrial revolution, the revival of the Japanese silk industry and an epidemic of viral and fungal diseases had pretty much shut down the European silk industry (Federico, 1997). We now know that the muscardine diseases are caused by the entompathogenic fungi Beauveria bassiana and Metarhizium anisipoliae, although this was not realised until the early part of the 19th Century when the Italian naturalist Agostino Bassi discovered their true nature.

So what about the aphids I hear you asking? I have written earlier about the attacks that aphids have to suffer from predators and parasitoids, but that is not all with which they have to contend.  Fungal diseases (Dean &Wilding, 1973; Rabasse et al., 1982; Aqueel & Leather, 2013) also attack aphids in the same way that they attack most other insects.  In the case of aphids, it is not one of the muscardines, instead they are attacked by a number of fungi belonging to the Entomophthoraceae. The first member of this family to be recognised as a fungus was named Empusa musca (now Entomophthora muscae) by Charles de Geer in 1782 (Cohn, 1855). As the name suggests, it attacks house flies. There are, however, a number of different entomopathogenic fungi that specialise in attacking aphids, Erynia neoaphidis, and other members of the Entomophtoraceae, being the most commonly seen (Dean & Wilding,

An aphid unfortunate enough to encounter an insect infecting fungal spore and lacking the appropriate symbionts (Parker et al., 2013) is very likely to suffer a slow and lingering death as the fungal mycelia proliferate within its body.

Aphid infected by Pandora (Erynia) neopahidis https://commons.wikimedia.org/wiki/File:Pandora_neoaphidis.jpg

Pandora neoaphidis infected pea aphids (photo Tom Pope)

On landing on a susceptible aphid, the fungal spore germinates and the germ tube penetrates the aphid, either directly through the cuticle or via a nearby spiracle.  Unlike those other invidious invaders of aphids, the parasitoids, entomopathogenic fungi need very specific environmental conditions to successfully colonise their aphid hosts. The damper the better, and if the aphid is surrounded by liquid water the more likely the fungus is to be able to effect an entry (Wilding, 1969; Dean & Wilding, 1973).  More than a century ago Paul Hayhurst of Harvard University noticed that galls of the Chenopodium aphid, Hayhurstia atriplicis (then known as Aphis atriplicis) that were ruptured and had allowed water in, had a much higher incidence of diseased aphids than the intact galls (Hayhurst, 1909). Another more recent indication of this dependence on damp conditions is a mention of a high incidence of Pandora neoaphidis (described as Empusa aphidis) on Schizolachnus pini-radiatae being associated with higher than average rainfall (Grobler, 1962). 

The earliest experiment involving aphid specific entompathogenic fungi that I have been able to find is from the latter half of the 19th Century (Houghton & Phillips, 1885). 

“I placed some infected aphides under a glass with healthy specimens from my garden-beans and in a short time these became similarly covered with the same red-coloured fungoid growth. The n*****s took the scarlet fever and died.”

Their conclusion was that it was an Entomopthora species, perhaps related to, if not, E. planchoniana.

Although fungal pathogens have been shown to be able to reduce aphid populations in the field (Fluke*, 1925; Grobler et al., 1962; Plantegenest et al., 2001), their effectiveness as biological control agents on their own is variable and unpredictable (Milner, 1997).  Most often, they are used either as biopesticides, or in conjunction with parasitoids and predators (e.g. Milner, 1997; Aqueel & Leather, 2013). One of the problems that entompathogenic fungi have is ‘finding’ their hosts.  While it is known that entompathogenic fungi, as with entomopathogenic viruses, affect the behaviour of many insect that they attack (Hughes et al., 2011), by making them move to locations on their host plant where they are more likely to infect their kin, as far as I know, there is only one record of this for aphids (Harper, 1958).  Surely a productive avenue of research to follow? That said, these clever fungi have another option up their mycelial sleeves.  They are, like other fungi, able to discharge their spores explosively.  Erynia neopahidis can project its spores more than 3mm vertically and more than 5 mm horizontally (Hemmati et al., 2001). This may seem a tiny distance to you and me, but the spores only need to get further than 2 mm to get air borne and move on to other plants or plant parts.  It might be a leap into the unknown but it seems to work out all right for the fungi 🙂

References

Aqueel, M.A. & Leather, S.R. (2013) Virulence of Verticillium lecanii (Z.) against cereal aphids; does timing of infection affect the performance of parasitoids and predators? Pest Management Science, 69, 493-498.

Cohn, F. (1855) Empusa muscae und die Krankeit der Stubenfliegen  Nova acta Academiae

Caesareae Leopoldino-Carolinae Germanicae Naturae Curiosorum, 25, 301-360

Dean, G.J. & Wilding, N. (1973) Infection of cereal aphids by the fungus Entomophthora. Annals of Applied Biology, 74, 133-138.

Federico, G. (1997 ) An Economic History of the Silk Industry, 1830-1930. Cambridge University Press, Cambridge.

Fluke, C.L. (1925) Natural enemies of the pa aphid (Illinoia pisi Kalt.); their abundance and distribution in Wisconsin.  Journal of Economic Entomology, 18, 612-616.

Grobler, J.H., MacLeod, D.M. & Delyzer, A.J. (1962) The fungus Empusa aphidis Hoffman parasitic on the wooly pine needle aphid, Schizolachnus pini-radiatae (Davidson). Canadian Entomologist, 94, 46-49.

Harper, A.M. (1958) Notes on behaviour of Pemphigus betae Doane (Homoptera: Aphididae) Infected with Entomophthora aphidis Hoffm. Canadian Entomologist, 90, 439-440.

Hayhurst, P. (1909) Observations on a gall aphid (Aphis atriplicis L.). Annals of the Entomological Society of America, 2, 88-100.

Hemmati, F., Pell, J.K., McCartney, H.A., Clark, S.J. & Deadman, M.L. (2001) Conidial discharge in the aphid pathogen Erynia neoaphidis. Mycological Research, 105, 715-722.

Hughes, D.P., Andersen, S.B., Hywel-Jones, N.L. , Himaman, W., Billen, J. & Boomsma, J. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology, 11, 13.

Milner, R.J. (1997) Prospects for biopesticides fro aphid control. Entomophaga, 42, 227-239.

Parker, B.J., Spragg, C.J., Altincicek, B. & Gerardo, N.M. (2013) Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity. Applied & Environmental Microbiology, 79, 2455-2458.

Plantegenest, M., Pierre, J.S., Dedryver, C.A. & Kindlmann, P. (2001) Assessment of the relative impact of different natural enemies on population dynamics of the grain aphid Sitobion avenae in the field. Ecological Entomology, 26, 404-410.

Rabasse, J.M., Dedryver, C.A., Molionari, J. & Lafont, J.P. (1982) Facteurs de limitation des populations d’Aphis fabae dans l’Ouest de la France 4. Nouvelles donnees sur le deroulement des epizooties entomophtoracees sur feverole de printemps. Entomophaga, 27, 39-53.

Roditakis, E., Couzin, J.D., K., B., Franks, N.R. & Charnley, R.K. (2000) Improving secondary pick up of insect fungal pathogen conidia by manipulating host behaviour. Annals of Applied Biology, 137, 329-335.

Wilding, N. (1969) Effect of humidity on the sporulation of Entomophthora aphidis and E. thaxteriana. Transactions of the British Mycological Society, 53, 126-130.

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Not all aphids live on the underside of leaves

If I were to misquote Jane Austen and state “It is a truth universally acknowledged, that aphids are found on the underside of leaves” most people who know what aphids are would agree without quibbling. If natural enemies could speak, they would probably agree as this quote from an early paper by my former boss, Hugh Evans puts it  “since most aphids are found on the lower surfaces of leaves anthocorids must be wasting time in searching the upper leaf surface” (Evans, 1976). The only enemies that regularly search the upper surface of leaves are parasitoids, which use aphid honeydew as a host-findng cue (e.g. Volkl, 1994), which is where it falls if the leaves above them are infested with aphids.  We know that not all aphids feed on leaves, many using roots, flowers, stems and even tree trunks as their preferred feeding sites, but do all leaf-feeding aphids behave in the same way?

A few species of leaf-dwelling aphid buck the trend and live on the upper surface of leaves. Dogma has it that most leaf-feeding aphids prefer the underside because there are more stomata there and this makes access to the phloem easier.

Aphis grossulariae on the underside of a gooseberry leaf, – only revealed because I turned the leaf over.

Look, however, at a neat experiment that Graham Hopkins and Tony Dixon did (Hopkins & Dixon, 2000). They showed that the birch aphid Euceraphis betulae, which is normally found on the lower surface of leaves, will, if the leaves are held so that the upper surface faces the ground, move from the now facing upward lower surface to the now facing downward upper surface. The answer can’t all be to do with the stomata. That said, in grasses and other monocotyledonous plants, there are more stomata on the upper surface of the leaves andmMany grass-feeding aphids do seem to have a predilection for the upper surface. The green spruce aphid, Elatobium abietinum, another aphid that has a very strong preference for feeding through stomata, is found mainly on the upper surface of spruce needles which are where the stomata are more prevalent (Parry, 1971).

Utamophoraphora humboltdi feeding on the upper surface of Poa annua outside my office.

The Green Spruce Aphid, Elatobium abietinum feeding on the upper surface of spruce needles (Albrecht (2017)

It is possible, however, that the preference for the upper surface of grasses is not entirely due to the relative abundance of stomata there.  The grass aphid, Sipha kurdjumovi for example, although most commonly found feeding on the upper surface of grass and cereal leaves, prefers to settle on a concave ridged surface (Dixon & Shearer, 1974), a characteristic of the upper surface of many grasses  Lewton-Brain, 1904). Another advantage to living on the upper surface of grass leaves is that when grasses want to conserve water they roll inwards along the mid-vein, which has the added benefit of hiding the aphids and protecting them from their natural enemies.

Mainly, however, if you are an aphid, you feed where the stomata are plentiful, hence the tendency for aphids living on monocotyledonous plants to feed mainly on the upper surface of leaves, instead of the lower surface.  Conversely, a leaf-feeding aphid on a dicotyledonous host plant would be expected to feed on the lower surface of the leaves, where there are more stomata.  It also makes sense for those aphids to be underneath the leaf, as there is less chance of them being knocked off by the rain or being dislodged by leaves brushing against each other in the wind.

There are, however, two tree-dwelling aphids in the UK that live on the upper side of the leaves of their woody hosts, the very rare Monaphis antennata on birch (Hopkins & Dixon, 1997) and the less rare large walnut aphid, Panaphis juglandis on walnut (Heie, 1982). So what makes these aphids so contrary? According to Graham Hopkins and Tony Dixon (Hopkins & Dixon, 1997), M. antennata is taking advantage of enemy-free space and to compensate for living on top of the leaf is cryptic to avoid detection by enterprising predators, and has a flattened and contoured body shape to avoid accidental dislodgement.

When it comes to P. juglandis things are bit more conjectural.  Interestingly, despite being a pest in some parts of the world (e.g. Wani & Ahmad, 2014) we don’t know much about it. It is also hard to understand why it has adopted the upper side of the leaf as its habitat.  One very obvious downside

Panaphis juglandis – prominently lined up along the mid-vein of the upper surface of a walnut leaf and displaying their possible unpalatability by their conspicuous yellow and black colouration.  From Influential Points  https://influentialpoints.com/Images/Panaphis_juglandis_nymphs_on-vein_c2013-07-06_18-35-17ew.jpg

is that by so doing it has opened Itself up to competition from the other common walnut aphid, Chromaphis juglandicola, the honeydew of which falls from the leaves like acid rain on to P. juglandis and prevents them living on the same trees (Olson, 1974; Wani & Ahmad, 2014).  In the absence of C. juglandicola it is, however, very successful with a number of life history traits that presumably ensure its survival, although no one has quantified this. First, it is striped yellow and black, a clear warning sign.  Bob Dransfield and Bob Brightwell who run that fantastic site, Influential Points, suggest that perhaps P. juglandis sequesters juglone from its walnut host as a defence against predators. It therefore makes sense to advertise it by being conspicuously coloured.  Second, they also, point out that the way in which the nymphs line up along the mid-vein might act as a form of masquerade mimicry or disruptive camouflage, by looking from certain angles like a blemish caused  by a fungal disease or injury. Neither of these suggestions answer the question as to why it lives on the upper side of leaves. For M. antennata, escape from natural enemies and competition are cited as the reason why it lives where it does.  Neither seem to explain P. juglandis, as it is not, at least according to Olson (1974), safe from predation and parasitism, although there is some indication that it might be ant-attended (Fremlin, 2016), nor is it able to share its host plant with the other walnut specialist, Chromaphis juglandicola. On the other hand, unlike M. antennata, it is most definitely not a rarity.

As they used to say when I was young, “answers on a postcard please”. In the meantime, until someone has the time and inclination to delve into this intriguing conundrum, I guess we should add it to Ole Heie’s list of unsolved aphid mysteries 🙂

 

References

Albrecht, A. (2017) Illustrated identification guide to the Nordic aphids feeding on conifers (Pinophyta) (Insecta, Hemiptera, Sternorhyncha, Aphidomorpha). European Journal of Taxonomy, 338, 1-160.

Dixon, A.F.G. & Shearer, J.W. (1974) Factors determining the distribution of the aphid, Sipha kurdjumovi on grasses. Entomologia experimentalis et applicata, 17, 439-444.

Evans, H.F. (1976) The searching behaviour of Anthocoris confusus (Reuter) in relation to prey density and plant surface topography. Ecological Entomology, 1, 163-169.

Fremlin, M. (2016) The large walnut aphid (Panaphis juglandis Goeze) – A few observations. Nature in North-East Essex, 2016, 68-76.

Heie, O.E. (1982) Fauna Entomologia Scandinavia, Vol. 11. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. II. The family Drepanosiphidae. Scandinavian Science Press, Klampenbourg, Denmark.

Heie, O.E. (2009) Aphid mysteries not yet solved/Hemiptera:Aphidomorpha./. Monograph Aphids and Other Hemipterous Insects, 15, 31-48.

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

Hopkins, G.W. & Dixon, A.F.G. (2000) Feeding site location in birch aphids (Sternorrhyncha: Aphididae): the simplicity and reliability of cues. European Journal of Entomology, 97, 279-280.

Lewton-Brain, L. (1904). VII. On the anatomy of the leaves of British grasses. Transactions of the Linnaean Society of London, Botany, Series 2, 6, 312-359.

Olson, W.H. (1974) Dusky-veined walnut aphid studies. California Agriculture, 28, 18-19.

Parry, W.H. (1971) Differences in the probing behaviour of Elatobium abietinum feeding on Sitka and Norway spruces. Annals of Applied Biology, 69, 177-185.

Volkl, W. (1994) Searching at different spatial scales: the foraging behaviour of the aphid parasitoid Aphidius rosae in rose bushes. Oecologia, 100, 177-183.

Wani, S.A. & Ahmad, S.T. (2014). Competition and niche-partitioning in two species of walnut aphids. International Journal of Scientific Research and Reviews 3, 120 – 125.

Willmer, C. & Fricker W (1996)  Stomata, Springer, Berlin.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Local – (101-300 UK hectad records)

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

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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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Not all aphids are extant – fossil aphids

Mention the word fossil and most people immediately think of dinosaurs, ammonites, early hominids and perhaps plants from the carboniferous.  For those of you who have coal-burning fires, have a look in your coal-scuttle, you may be surprised at what you find.  What most people don’t realise is that there are fossil insects and these include those fabulous insects, aphids 🙂

A beautifully preserved aphid, Mindarus harringtoni, named after, and owned by my friend, and fellow aphid enthusiast, Richard Harrington.

The oldest fossil of a true insect dates back to the Pragian (early Devonian) era (396-407 million years ago (Mya)) implying that they can, almost certainly, be dated back to the earlier Silurian period (434 Mya) (Engel & Grimaldi, 2004). Aphids, being relatively soft-bodied animals, tend to be less commonly found as stone fossils, but there are some fine examples in existence.  The oldest aphid fossil found so far is Vasegus triassicus from the Vosges area of France and dating back to 174-163 Mya (Szwedo & Nel, 2011).  I have a great admiration for taxonomists in general, but paleoentomologists really are worthy of worship, working as they do, with material, especially that found in rock deposits, of an extremely taxing nature.

Wing of the aphid Vosegus triassicus  (Szwedo & Nel, 2011)

A more recognisable aphid wing from the Lower Cretaceous (140 Mya).  https://jurassiccoast.org/fossilfinder/1338-aphid-wing/

Another contender for the oldest aphid was found in the Daohugou beds in China on the boundaries of the provinces of Inner Mongolia, Hebei and Liaoning (Huang et al., 2015).  These deposits have been dated back to about 165 Mya.  Given the inevitable distortion caused by the squashing, the fossils do look like some modern aphids and I am pretty certain that I can see the cauda which is one of the distinguishing characteristics of aphids.

Daopaphis magnalata with a visible cauda? (Huang et al., 2015)

Somewhat younger, a mere 15 000 000 years old, Palaeogreenidea rittae, which displays the other dead giveaway that tells you that you are looking at an aphid, the siphunculi.

Palaeogreenidea rittae, note the distinctive siphunculi.  Middle Miocene from Nevada (approximately 15 Mya) (Heie, 2006).

Amber, fossilised tree resin, is, however, where you are most likely to find ancient aphids.  Tree resin is a carbohydrate-based extremely sticky secretion of trees, particularly conifers. It is part of their defence system and is used to seal wounds and to trap and encapsulate any insect intent on forcing an entry into the heart of the tree. The majority of the insects found in resin have arrived there by accident; they have landed on it and found themselves trapped.  They gradually become engulfed by the resin and die a slow and lingering death, unless a bird plucks them from their sticky surroundings as a tasty snack.  Go into a pine forest or look at the resin bleeds that you often find on fruit trees and you will very soon find some hapless insect victims. Over time the resin hardens and becomes a substance known as copal.  This can then find its way into the soil; the tree falls over or the copal becomes detached and falls to the round. Once in the soil, the copal has the chance, over several million years, to harden further still and eventually become resin.  Any insect trapped in resin is perfectly preserved, ready for the intrepid palaeoentomologist to discover and name or entrepreneur to sell to curio collectors.

A very fine specimen with a very long stylet; presumably this fed on the trunk of trees.  Germaraphis spp. (Pemphigidae)    http://www.fossilmuseum.net/Fossil-Amber/antaphid/amber-86.htm 

 

A very recognisable aphid indeed, the antennal tubercles, siphunculi and cauda are all very clear.  Photo from Ross (2009).

Not all aphids in amber are as easy to identify as the two specimens above.  The example below is why I have such a great admiration for palaeoaphidologists.

I am told that this is an aphid.  Photographed and found by Gracie Price a placement student at Oxford University Museum of Natural History, reproduced with thanks to Darren Mann.

I have written earlier about the close relationships that many aphids have with ants and it seems from the number of times ants and aphids have been found in close proximity in amber inclusions, that this association has been in existence for at least 73 million years especially with Germaraphis dryoides (Heie, 1967; Perkovsky, 2009).

Ant and aphid in amber. It will cost you €100 if you want to own this specimen.  http://www.amberinclusions.eu/ant-and-aphid-symbiosis-in-baltic-amber-4809#prettyPhoto

Another association, perhaps not so pleasant for the aphid, and also immortalised in amber, is that of a nematode parasite from 100 million years ago (Poinar, 2017).

Aphid in amber with nematode parasite (Poinar, 2017).

What can we learn from these amber inclusions?  First, by comparing them with modern aphids, we can make inferences about their life styles.  As Ole Heie (1967) pointed out, aphids with clawed tarsi (feet) and long mouth parts are almost certainly not only to be tree dwellers, but ones that fed through the bark on the stems or trunks.  Aphids that live on the underside of leaves need neither of these adaptations.  Are there any other inferences to be made? I have already pointed out that, the fossil evidence suggests the ant-aphid mutualism has been long-established.

Fossil aphids also allow us infer that as aphids are largely found in temperate zones, the climate in those sites where amber is easily found must also have been temperate when they were trapped by the then, fresh tree resin (Heie, 1967).  Palaeobiologists have attempted to reconstruct ancient ecosystems from fossils including insects.  A recent and innovative study comparing arthropods found in trapped in modern tree resins, sticky traps and Malaise traps with those in fossil amber suggests that amber inclusions reflect the insects closely associated with trees but not necessarily the overall community (Kraemer et al., 2018).  We can’t get DNA out of amber as suggested in Jurassic Park, but we can certainly get a lot of other biological information from this fantastic window into the past.

I’ll end on a cautionary note. Not all amber is real amber.  Fakes abound.  Plastic is often used as fake amber and is sold with insect inclusions or as jewellery.  An easy way to test if it is plastic or amber, is to see if it floats in a saturated salt solution, if it does it is probably amber. More difficult to detect, is fake amber that has been produced by melting down real amber or copal, and then had modern insects embedded in it while it is still liquid.  If your insect inclusion is very nicely and symmetrically arranged, then you can be sure it is a fake.  Not all such inclusions are sold as genuine, most openly advertise exactly what they are; I have several, gifts from families and students.

Modern insect embedded in plastic.

 

References

Engel, M.S. & Grimaldi, D. (2004) New light shed on the oldest insect. Nature, 427, 627-630.

Heie, O. (1967) Studies on Fossil Aphids (Homoptera: Aphidoidea) Especially in the Copenhagen Collection of Fossils in Baltic Amber. Spolia Zoologica Musei Hauniensis, Copenhagen.

Heie, O.E. (2006) Fossil aphids (Hemiptera: Sternorrhyncha) from Canadian Cretaceous amber and from the Miocene of Nevada. Insect Systematics & Evolution, 37, 91-104.

Huang, D., Wegierek, P., Żyła, D. & Nel, A. (2015) The oldest aphid of the family Oviparosiphidae (Hemiptera: Aphidoidea) from the Middle Jurassic of China. European Journal of Entomology, 112, 187-192.

Kraemer, M.M.S., Declos, X., Clapham, M.E., Arillo, A., Peris, D., Jäger, P., Sebner, F., Peñalver, E. (2018) Arthropods in modern resins reveal if amber accurately recorded forest arthropod communities. Proceedings of the National Academy of Sciences, USA, 115, 6739-6744

Perkovsky, E.E. (2009) On finding a single-clawed aphid, Germaraphis ungulata (Homoptera, Aphidinea), in a syniclusion with the ant Monomoroium mayrianum (Hymenoptera, Formicidae) in the Saxonian amber.  Paleontological Journal, 43, 1006-1007.

Poinar, G.O. (2017) A mermithid nematode, Cretacimermis aphidophilus sp. n. (Nematoda: Mermithidae) parasitizing an aphid (Hemiptera: Burmitaphididae) in Myanmar amber: a 100 million year association.  Nematology, 19, 509-513.

Ross, A. (2009) Amber – The Natural Time Capsule. NHM, London.

Szwedo, J. & Nel, A. (2011) The oldest aphid insect from the Middle Triassic of the Vosges, France. Acta Palaeontologica Polonica, 56, 757-766.

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Aphids don’t suck sap! (usually)

Aphids are sap feeding, most of the time they feed from the phloem, or sieve elements, that part of the plant responsible for transporting the food made in the leaves by photosynthesis, around the plant.  Aphids face three problems arising from their phloem feeding habit. First, the phloem sap is largely composed of sugars, with a few trace elements and nitrogen in the form of soluble amino acids.  The aphids are mainly interested in the nitrogen and that poses the second problem, the amino acids are mainly non-essential ones.  Thirdly, the phloem is under pressure, figures range from 2 to 40 Bars* (about twice to forty times atmospheric pressure) (e.g. Mittler, 1957; Rogers & Peel, 1975; Barlow & Randall, 1978; Wright & Fisher, 1980).  Imagine that you are trapped in an air-tight room and your only source of air is an inflated tractor tyre.   You have a sharp metal straw which you can stick into the tyre to release the air into your mouth.  If you put one end of the straw in your mouth and then pierced the tyre wall, your head would explode.

Sadly I couldn’t find a picture of an exploding aphid and my cartoon version was a failure, so this is it 🙂

Aphids face the same sort of pressure. Fortunately evolution has provided them with a very strong pharyngeal pump and incorporated a series of valves in their mouth-parts (stylets = straw) with which they are able to control the flow of the phloem into their bodies.  The last thing they want to do when plugged into the phloem is suck, it would be the last thing they did 🙂 and that’s why aphidologists get upset when people describe aphids as sap-suckers!

 

Aphid feeding apparatus – adapted from McLean & Kinsey (1984)

To be fair, we are being somewhat pedantic, the fluid transported in the xylem tubes, largely water, is also colloquially known as plant sap. The xylem, unlike the phloem is not under pressure (Sperry et al., 1996), so on those rare occasions when the aphid does need to drink water, they do have to suck sap (Spiller et al., 1990).  The other occasion on which aphids need to suck rather than regulate the flow of sap is when they are feeding in very artificial laboratory situations, on leaf discs or on artificial diets where the nutrient solution is between two pieces of Parafilm™.  In both these cases there is negative pressure and the cibarial pump does then come into operation. Interestingly, it is sometimes quite difficult to get aphids to feed on artificial diets unless a phagostimulant is included to overcome their reluctance to feed on sap that is not under pressure (Mittler & Dadd, 1963), but that’s a story for a future post.

Aphids feeding on leaf discs, in this case for insecticide assays at Rothamsted Research

 

Aphids feeding on artificial diet through Parafilm™. Photo Meena Haribal https://www.sciencedaily.com/releases/2015/12/151216151742.htm

 

References

Barlow, C.A. & Randolph, P. A.  (1978) Quality and quantity of plant sap available to the pea aphid.  Annals of the Entomological Society of America, 71, 46-48.

McLean, D.L. & Kinsey, M.G. (1984) The precibarial valve and its role in the feeding behavior of the pea aphid, Acyrthosiphon pisum. Bulletin of the Entomological Society of America, 30, 26-31.

Mittler, T.E. (1957) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae) I. The uptake of phloem sap. Journal of Experimental Biology, 34, 334-341.

Mittler, T.E. & Dadd, R.H. (1963) Studies on the artificial feeding of the aphid Myzus perslcae (Sulzer) – I. Relative uptake of water and sucrose solutions. Journal of Insect Physiology, 9, 623-645.

Sperry, J.S., Saliendra, N.Z., Pockman, W.T.,  Cochard, H., Cruiziat, P., Davis, S.D., Ewers, F.W. & Tyree, M.T. (1996) New evidence for large negative xylem pressures and their measurement by the pressure chamber method. Plant, Cell & Environment, 19, 427-436.

Rogers, S. & Peel, A.J. (1975) Some evidence for the existence of turgor pressure gradients in the sieve tubes of willow Planta (Berl.) 126, 259-267.   

Spiller, N.J., Koenders, L. & Tjallingii, W.F. (1990) Xylem ingestion by aphid – a strategy for maintaining water balance.  Entomologia experimentalis et applicata, 55, 101-104.

Wright, J.P. & Fisher, D.P. (1980) Direct measurement of sieve tube turgor pressure using severed aphid stylets. Plant Physiology, 65, 1133-1135.

 

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Entomological classics – Aphids spit: visualising aphids feeding, the electrical penetration graph

Aphids as a taxonomic group, have been recognised since at least 1758 when Linnaeus coined the genus Aphis and have been cited as important pests for more than 200 years “The Aphis or Blighter, as we now for the first time venture to call it, from its being the most general cause of what are termed blights in plants..” (Curtis, 1802).  A detailed understanding of how they fed, was however, longer in being reached, but by 1914 the anatomy of the aphid mouthparts and the process of stylet insertion was fully described (Davidson, 1914).  Davidson (1923) also described the role that aphid saliva plays in helping the aphid feed by making it easier for the stylet to move between cells on its convoluted journey to the phloem, made visible as the so-called stylet tracks.

Drawings showing the effects produced by the passage of aphid stylets of three different aphid species through leaf tissue (Davidson, 1923).

Fast forward a couple of years and we have intrepid entomologists producing photographic evidence of aphid stylets in action (Smith, 1926).

Photomicrographs of the stylet of Myzus persicae in situ and the resultant stylet track (Smith, 1926).

One of the reasons that applied entomologists were so interested in aphid feeding was the role that aphids, and other insects, played as vectors of plant viruses, which until the 1920s, was not formally proven (e.g. Kunkel, 1926, Smith, 1926, 1929). You would be forgiven for thinking that once the connection between aphid feeding and plant virus transmission had been demonstrated then that would be it.  But no, much wants more, and aphidologists became intrigued about the link between aphid feeding and salivation, in particular when and exactly where these activities occurred in the plant.  Those entomologists working on plant viruses wanted to know which part of the feeding process was linked to the acquisition and inoculation of the viruses from and to the aphid host plant.  A possible solution to these conundrums, was, however, on the horizon.

In the early 1960s, two entomologists from the Department of Entomology, at the University of California, Davis, Donald McLean and Marvin Kinsey,  came up with a system that was to revolutionise the study of the feeding behaviour of aphids and other insects that feed internally on plant using piercing mouthparts (McLean & Kinsey, 1964). In essence, what they did was to make an aphid part of an electrical circuit by attaching a thin copper wire to its back using a quick-drying silver paint.  The feeding substrate, a leaf, had a 2.0 Volt, 60-cycle alternating current introduced to it and this was placed on an insulated grid connected to an amplifier connected in parallel with an oscilloscope, a chart-recorder and a speaker. The wire attached to the aphid, was joined to the grid and when the aphid began to feed this completed the circuit, and changes in voltage were able to be observed and recorded.  The next step was to identify which chart recordings were associated with sap ingestion and salivation by the aphid.  Using an artificial leaf, Parafilm stretched over a well containing a sucrose solution, and watching the aphids under a high power microscope, these innovative entomologists were able to identify four different stages involved in aphid feeding (Mclean & Kinsey, 1965).

The ground-breaking chart recording (Mclean & Kinsey, 1965) and as you might expect it was a pea aphid 🙂

 

A visual summary of what McLean and Kinsey were watching and recording (from Dixon (1973).

Not satisfied with these findings McLean and Kinsey modified their equipment and intensified their observations, sacrificing a number of aphids in the process.  When different waveforms were seen the poor aphids had their stylets amputated and the plant material with the stylet still in place was then examined under a high power microscope.  This meant that they were able to definitively correlate their recordings with the position of the stylet in different leaf tissues and during different behaviours (McLean & Kinsey, 1967).  As well as trying to understand how, when and where plant viruses were acquired or transmitted, it turns out that using the waveforms generated by the aphid mouthparts as they weave their way through the leaf tissues, is not only a useful way of assessing the resistance mechanism of a plant (e.g. Nielson & Don, 1974; Paul et al., 1996; ten Broeke et al., 2016) but also for detecting resistance to insecticides (e.g. Garzo et al., 2016).

Modifications to the original equipment happened very quickly; by 1966, a more compact and easier to use version using Direct Current had been developed (Schaefers, 1966). That said, the first correlation of a specific waveform and virus acquisition by the pea aphid, was shown using the original AC equipment (Hodges & Mclean, 1969).  A further modification of the Schaefers DC equipment was developed during the 1970s, such that test aphids were able to live and reproduce for up to ten days whilst attached to the set-up, thus allowing very detailed investigation of the correlations between the electrical signal patterns produced and the feeding behaviours of the aphids (Tjallingii, 1978).

Those of you who take note of such things, will have noticed, that so far, some 14-years after its invention, the term electrical penetration graph has not yet appeared, either here or in the scientific literature.   Earlier references to recordings using the technique use the term actograph which was somewhat non-specific, as it refers to any graphical representation of behavioural activity.  So when did the term Electrical Penetration Graph (EPG) first appear in the literature.  Google Scholar gave me a date of 1984 from a paper looking at the resistance of lettuce to the cabbage aphid Brevicoryne brassicae, a paper that includes Freddy Tjallingii in the authorship list (Mentink et al., 1984).  In this paper the authors refer to a conference proceedings paper (Tjallingii, 1982) as being the source of the name.  On tracking down that paper I found that it doesn’t actually mention the term EPG.  The first paper that specifically mentions and defines the term as “the recorded graph as a result of an overall electrical signal caused by stylet penetration activities” is Tjallingii (1985).  Strangely the author introduces the term thus “Here we introduce the term ‘electrical penetration graph (EPG)”, which I found slightly odd as it is a single author paper 😊  Inputting EPG or electrical penetration graph into Web of Science shows an increasing number of papers using and mentioning the technique, but surprisingly the first paper recorded is from 1999.

NGram finds the first mention slightly earlier, 1981.  A puzzle waiting to be solved for anyone with the time or inlcination.

The frequency of the occurrence of the phrase “Electrical penetration graph” according to Ngram Viewer (accessed and downloaded May 1st 2018).

The technique is now very well established and used around the world.  The equipment is commercially available through EPG Systems, which is where we got ours from and just in case you were wondering, this is what it looks like.

Faraday Cage (an earthed metal screen) surrounding the equipment to exclude electrostatic and electromagnetic influences

Our test plants in situ connected up to the electrical supply, recording equipment and amplifier.

Close up of the plants and EPG electrodes

Aphids connected up to the EPG. Photo courtesy of https://sites.google.com/site/ezwear1/epgIMG_0903.jpg

A simple guide to interpreting the waveforms

http://www.epgsystems.eu/file/46-waveform-features

For Open Days and public displays it is not unknown for mischievous entomologists to link particular waveforms to recordings of sucking and spitting sounds and to play these back when the equipment is being demonstrated 🙂

 

References

Curtis, W.L. (1802) IV. Observations on aphides, chiefly intended to show that they are the principal cause of blights in plants, and the sole cause of the honeydewTransactions of the Linnaean Society of London, 6, 75-94.

Davidson, J. (1914) On the mouth-parts and mechanism of suction in Schizoneura lanigera, Hausmann. Zoological Journal of the Linnaean Society, 32, 307-330.

Davidson, J. (1923) Biological studies of Aphis rumicis Linn. The penetration of plant tissues and the source of the food supply of aphids.  Annals of Applied Biology, 15, 35-54.

Gabrys, B., Tjallingii, W.F. & van Beek, T.A. (1997) Analysis of EPG recorded probing by cabbage aphid on host plant parts with different glucosinolate contents. Journal of Chemical Ecology, 23, 1661-1673.

Garzo, E., Moreno, A., Hernando, S., Marino, V., Torne, M., Santamaria, E., Diaz, I. & Fereres, A. (2016) Electrical penetration graph technique as a tool to monitor the early stages of aphid resistance to insecticides. Pest Management Science, 72, 707-718.

Hodges, L.R. & McLean, D.L. (1969) Correlation of transmission of Bean Yellow Mosaic Virus with salivation activity of Acyrthosiphon pisum (Homoptera: Aphididae). Annals of the Entomological Society of America, 62, 1398-1401.

Kunkel, L.O. (1926) Studies on Aster Yellows. American Journal of Botany, 13, 646-705.

McLean, D.L. & Kinsey, M.G. (1964) A technique for electronically recording aphid feeding and salivation. Nature, 202, 1358-1359.

McLean, D.L. & Kinsey, M.G. (1965) Identification of electrically recorded curve patterns associated with aphid salivation and ingestion. Nature, 205, 1130-1131.

McLean, D.L. & Kinsey, M.G. (1967) Probing behavior of the pea aphid, Acyrthosiphon pisum. I. Definitive correlation of electronically recorded waveforms with aphid probing activitiesAnnals of the Entomological Society of America, 60, 400-405.

Mentink, P.J.M., Kimmins, F.M., Harrewijn , P., Dieleman, F.L., Tjallingii, W.F.,  van Rheenen, B. &  Eenink, A.H. (1984)  Electrical penetration graphs combined with stylet cutting in the study of host plant resistance to aphids. Entomologia experimentalis et applicata, 35, 210-213.

Nielson, M.W. & Don, H. (1974) Probing behaviour of biotypes of the spotted alfalfa aphid on resistant and susceptible and alfalfa clones.  Entomologia experimentalis et applicata, 17, 477-486.

Paul, T.A., Darby, P., Green, C.P., Hodgson, C.J. & Rossiter, J.T. (1996) Electrical penetration graphs of the damson-hop aphid, Phorodon humuli on resistant and susceptible hops (Humulus lupulus).  Entomologia expeimentalis et applicata, 80, 335-342.

Powell, G. (1991) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Annals of applied Biology, 119, 313-321.

Schaefers, G.A. (1966) The use of direct current for electronically recording aphid feeding and salivation. Annals of the Entomological Society of America, 59, 1022-1024.

ten Broeke, C.J.M., Dicke, M. & van Loon, J.J.A. (2016) Feeding behaviour and performance of Nasonovia ribisnigri on grafts, detached leaves, and leaf disks of resistant and susceptible lettuce.  Entomologia experimentalis et applicata, 159, 102-111.

Tjallingii, W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia experimentalis et applicata, 24, 521-530.

Tjallingii, W.F. (1982) Electrical recording of aphid penetration. [In] J.H. Visser & A.K. Minks (eds.) Proceedings of the 5th Symposium on Insect Plant-Relationships, 1-4 March, 1982, Wageningen, Pudoc, pp 409-410.

Tjallingii, W.F. (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia experimentalis et applicata, 38, 177-185.

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

Smith, K.M. (1929) Studies on potato virus diseases, V. Insect transmission of potato leaf roll.  Annals of Applied Biology, 16, 209-229

 

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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-cadavershttp://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 parasitoidsEntomologia 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 rhopalosiphiEntomologia 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 SulzerPhysiological 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.

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

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