Time of year determines some, but not all, views of my blog posts

I was going to format this post as a spoof Nature communication, but not being as skilled as our students, who turn out excellently formatted mock papers for their assignments, decided not to. I did, however, go for a typical Nature title 🙂

The other day when I was looking at my blog stats I clicked on the view post stats button next to my most read post of the day, Not all aphids are vegans*, and was amused enough by the strong seasonal dynamics shown to post it on Twitter.

Not all aphids are vegans – strong seasonal dynamics

As you can see, the peaks and troughs of views strongly follow the times of year that aphids are present and absent.

As regular readers of my blog will know, I am a bit of an aphidophile. It is kind of hard to miss if I’m honest, but then aphids are fantastic and awesome, so you will get no apologies from me for loving them and writing, or talking about them whenever I get the chance to do so.

That said, not all my posts are about aphids, insects yes, but I do write about other things too, including entomological equipment, classic papers and teaching matters, and sometimes about my holidays 🙂

Given the strong correlation between aphid life cycle timing and visits to the post about biting aphids, I wondered how my other aphid posts stacked up in terms of seasonal viewing.

Aphid life cycles – bizarre, complex or what?

Somewhat surprisingly, well to me at least, the post about aphid life cycles did not show very strong seasonal dynamics, although April, when aphids start to become active, did, at the beginning of the post’s life, show a bit of a peak of interest, but has since broken down completely.  Another season aspect of aphid biology is wing formation. This is usually associated with late spring and early summer (Dixon, 1973, 1976), and in this case, the viewing history fitted appropriately.

Not all aphids have wings – seasonally appropriate

 

What about the other end of the year, autumn and winter?  As expected, my post about aphid overwintering showed the reverse pattern to the other aphid posts, people wanted to read about aphid overwintering as winter appraoched.

A Winter’s Tale – aphid overwintering

Aphid posts, as predicted, show a correlation (OK, not tested) with the time of year associated with the appropriate part of the life cycle.  We would therefore expect that posts that are more general would show no marked seasonality in their popularity. To test this I looked at first, my posts that deal with entomological equipment, pan traps, clip cages and the poster and then at two posts that fit into the teaching category.  Staring with the Pan trap, a very basic and commonly used piece of field equipment, despite a slight expectation on my part that there might be a spring peak (after all, that is when insects start flying) there was no pattern that I could see.

The pan trap – disappointingly no pattern

 

Nest I looked at the Pooter, an essential bit of general entomological kit (Leather, 2015) used by entomologists of all types. Given that this is used in both the laboratory and the field, I didn’t really expect to see any pattern jumping out at me.  I wasn’t disappointed although if you look very quickly, and not too closely, it is just about possible top convince yourself that there is an increase in views during the summer, which would fit with the general increase in insects caught in nets.

The Pooter – perhaps a slight tendency for views to increase in mid-summer

 

Next, back to aphids, this time a piece of kit that is almost, but not entirely, confined to aphidologists (Macgillivray & Anderson, 1957).  My expectation here, was that given that clip cages are almost always used in laboratories or glasshouses, that there would be absolutely no pattern in the viewing figures. Sure enough, that was the outcome.

The clip cage – no discernible patterns

Finally, the two teaching posts, first my tribute to Southwood’s classic species-area paper (Southwood, 1961).  I know that this post is used for undergraduate teaching at one university, so given the regularity of university timetabling, might have a chance of  showing a pattern;  It didn’t.

Southwood (1961) – the number of insect species associated with various trees – no pattern

Finally, a post that has attracted a modicum of attention over the years, all about what to expect in a PhD viva.  My hypothesis for this, given that most PhD projects start at the beginning of the academic year and run for four or five years before submission, was that if there was going to be an annual peak in views that it would be between October and January.  To save you the troubkle of squinting at the graph, there was no pattern.

Are PhD examiners really ogres? – no consistent peak

In conclusion, aphid posts tend to show viewing patterns consistent with the time of year and life cycle stage, other, more general posts show absolutely no pattern.

 

References

Dixon, A.F.G. (1973) Biology of Aphids. Edward Arnold, London.

Dixon, A.F.G. (1976) Reproductive strategies of the alate morphs of the bird cherry-oat aphid Rhopalosiphum padi. Journal of Animal Ecology, 45, 817-830.

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

MacGillivray, M.E. & Anderson, G.B. (1957) Three useful insect cages. Canadian Entomologist, 89, 43-46.

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

 

*which I have purposely not linked to so as to not influence the count!

 

 

 

Not all aphids are farmed by ants

One of the great things about working with aphids is that it gave me the chance to go back to my childhood entomological roots of playing with ants.  Most gardeners have had the experience when cruelly* running their finger and thumb down an aphid covered plant stem of finding their hand suddenly covered with ants.   As someone who has a very relaxed approach to aphids, I find the presence of ants on a plant a handy way of finding aphids, although sometimes the ants are there because of extra-floral nectaries.  So what exactly is going on when you find ants and aphids together?

It has long been known that some aphids are farmed or tended by some ant species.  According to Jones (1927) Goedart** was the first to describe the relationship scientifically (Goedart & Lister, 1685) and by the latter half of the 19^th Century you can find illustrations such as the one below that appeared in Van Bruyssel’s fantastic foray into early science-communication.

An ant dairy maid coming to milk her aphids – their siphunculi and anuses are just visible if you look closely: cleverly made to look like cow heads (From Van Bruyssel, 1870)

The ant-aphid association is usually defined as a mutualism as the two species exist in a relationship in which each individual benefits from the activity of the other.  Just to confuse people however, the association is also sometimes termed trophobiosis*** (e.g. Oliver et al., 2008) which is a more symbiotic relationship.

The degree of dependence of the aphid on the ants varies from species to species.  Some aphids, especially those that live underground on plant roots, are unable to survive without their ant attendants (Pontin, 1978).   Pontin (1960) also reports seeing Lasius flavus workers licking aphid eggs which he suggests stops them from going mouldy as the licking removes fungal spores.  He also noted that those eggs that were not cared for in this way did not hatch.  Other aphids have a more facultative relationship, and are able to survive quite successfully without the help of their friendly neighbourhood ants.

We tend to think of aphids as soft squidgy defenceless things that are easy to squash.  To other insects however, they present a bit more of a challenge.  Aphids have structural and behavioural defences to keep them safe in the dangerous world of bug eat bug.  Alarm pheromones and dropping behaviour are commonly used by aphids to avoid meeting predators face to face (Dixon, 1958a).    Aphis also have a number of physical defences.  Their spihunculi (cornicles) can produce a quickly hardening wax to gum up ladybird jaws (Dixon, 1958b).  Other aphid species cover themselves with dense waxy coats that make them less palatable or accessible to natural enemies (Mueller et al., 1992).  Other aphids have thick skins (heavily sclerotized) and what entomologists term saltatorial leg modification; long legs to you and me, and so able to give a ladybird or other opportunistic insect predator a good kicking (Villagra et al., 2002).  These characteristics, which are all costly, are reduced or absent in aphids that are frequently associated with ants (Way, 1963) as presumably with ant bodyguards in attendance, there is no need for the aphids to invest in extra anti-predator defences.

Note also the shortened siphunculi in Periphyllus testudinaceus and the hairier bottom, when compared with the leggy, and arguably, prettier Drepanosihpum platanoidis.

Apart from reducing their defensive armoury, those aphids that are obligately ant attended have a specially adapted rear end, essentially a hairy bottom.  This is more scientifically known as the trophobiotic organ.   The trophobiotic organ is an enlarged anal plate surrounded by special hairs that acts as a collection and storage device that allows the aphid to accumulate honeydew ready for the ants to remove at their leisure.

Three different trophobiotic organs, some hairier than others – after Heie (1980)

A real live view of the “trophobiotic organ” of Tetraneura ulmi (from the fantastic Influential Points website – http://influentialpoints.com/Images/Tetraneura_ulmi_aptera_on_grass_roots_c2015-09-04_14-53-13ew.jpg

Non-ant attended aphids without the trophobiotic organ, deposit their honeydew directly on to the leaf surface or on the ground, or if you are unlucky enough to park under an aphid infested tree, on to your car 🙂  Ants lick and collect sycamore aphid, Drepanosiphum platanoidis honeydew from leaves, but not directly from the aphids, which they do do from the maple aphid, Periphyllus testudinaceus, which also lives on sycamore trees P. testudinaceus (Pontin, 1958).

So what’s in it for the ants?  Why should they bother looking after aphids, even in some cases, keeping aphid eggs in their nests over the winter (Pontin, 1960)? The obvious answer is the honeydew that the aphids produce as a by-product of feeding on phloem sap. The amount of material that an aphid can remove from a plant is quite astounding.  A large willow aphid (Tuberolacnhus salignus) adult can sucks up the equivalent of 4 mg sucrose per day Mittler (1958) , which is equivalent to the photosynthetic product of one to two leaves per day.  Admittedly, they are large aphids and not ant attended****, but even an aphid half their size passes a lot of plant sap through their digestive systems.  Honeydew is not just sugar but is a mixture of free amino acids and amides, proteins, mineral and B-vitamins, so all in all, quite a useful food source for the ants (Way, 1963).  All aphids produce honeydew but not all aphids are ant attended and as I pointed out earlier, not all ants attend aphids.  Our research suggests that 41% of ant genera have trophobiotic species, but these are not equally distributed among ant families.  Some ant sub-families, for example the Fomicinae,  specilaise in ant attendance,  whereas in other ant families such as the Ecitoninae, aphids are used only as prey and the honeydew is gathered from plant and ground surfaces (Oliver et al., 2008).  The ant species that are most likely to develop mutualistic relationship with aphids appear to be those that live in trees, have large colonies, are able to exploit disturbed habitats and are dominant or invasive species (Oliver et al., 2008).

Those ants that do tend aphids don’t just protect them from predators and other natural enemies. They want to maximise the return for their investment. The black bean aphid, Aphis fabae, which is often tended by Lasius niger, has its tendency to produced forms reduced by the ants, thus making sure that the aphids are around longer to provide food for them (El-Ziady & Kennedy, 1956).  The ant Lasius fuliginosus transports young Stomaphis quercus aphids to parts of the tree with the best honeydew production (Goidanich, 1959) and Lasius niger goes one step further, moving individuals of the aphid Pterocomma salicis, to better quality willow trees (Collins & Leather, 2002).  Lasius niger seems to have a propensity for moving bugs about, they have also been seen moving coccids from dying clover roots to nearby living ones (Hough, 1922).

In the mid-1970s John Whittaker and his student, Gary Skinner, set up a study to examine the interactions between the wood ant, Formica rufa and the various insect herbivores feeding on the sycamore trees in Cringlebarrow Wood, Lancashire.  They excluded some ants from some of the aphid infested branches and allowed them access to others on the same trees and also looked at trees that were foraged by ants and those that weren’t.  They found that F. rufa was a heavy predator of the sycamore aphid, D. platanoidis, but tended the maple aphid,  P. testudinaceus (a novel observation for that particular ant-aphid interaction).  Ant excluded colonies of P. testudinaceus decreased, whereas D. platanoidis did not, but on those branches where ants were able to access the aphids, the reverse pattern was seen (Skinner & Whittaker, 1981).

The presence of thriving aphid colonies in the neighbourhood of ant nests and in some cases aphid colonies only exist where there are ant nests nearby (Hopkins & Thacker, 1999), has made some people wonder if aphids actively look for ant partners (Fischer et al., 2015).  There is, however, no evidence that aphids look for ant partners, rather the fact that wing production is reduced in the presence of tending ants, means that aphid colonies can accumulate around and close to ant nests (Fischer et al., 2015a).

That doesn’t mean that the aphids only rely on honeydew production to guarantee the presence of their ant bodyguards. The aphid Stomaphis yanonis, which like other

Stomaphis aceris, also ant attended.  Imagine trying to drag that mouth part out of a tree trunk quickly 🙂

Stomaphis species, has giant mouthparts, and so needs plenty of time to remove its mouthparts safely definitely needs ant protection to cover its back when involved in the delicate operation of stylet unplugging. In this case, it turns out that the aphids smell like that ants, they have cuticular hydrocarbons that resemble those of their ant protector Lasius fuji and thus encourages the ants to treat them as their own (Endo & Itino (2013).  Earlier work on the ant-attended tree-dwelling aphids, Lachnus tropicalis and Myzocallis kuricola, in Japan showed that the ant Lasius niger preyed on aphids that had not been attended by nest mates, but tended those that had been previously tended (Sakata 1994).  This too would indicate the presence of some sort of chemical marker or brand.

To add support to this, just over twenty years ago (1996), I supervised an undergraduate student Arran Frood*****.   He worked with the maple aphid, and the ants L. niger and L. fulginosus.  Aphids on ant-attended sycamore trees were washed with diluted acetone or water.   Those that had been washed with acetone were predated more than unwashed aphids suggesting that It was like washing off the colony specific pheromone marker. In support of this hypothesis, Arran found that predation would also increase if he swapped a twig full of aphids between colonies, but not from one part of the colony to another. It also worked between the two ant species, Lasius niger and L. fuliginosus, so it seems like the ants have a colony specific marker on their aphids.  We should really have written this up for publication.

Although aphids do not actively seek ant partners, they may compete with each other to retain the services of their ant bodyguards by producing more honeydew (Addicott, 1978).  There is evidence that ants make their decisions of whether to predate or tend aphids by monitoring honeydew production and choose to prey on aphids in colonies that produce less honeydew (Sakata, 1995).  Recent work has also shown that the honeydew of the black bean aphid, Aphis fabae is often colonised by the bacterium Staphylococcus xylosus. Honeydew so infected produces a bouquet of volatile compounds that are attractive to the ant L. niger thus increasing the cahnces of the aphids being ant-attended (Fischer et al., 2015b).  This adds yet another layer of complexity to the already complicated mutualistic life style that aphids have adopted.

And finally, you may remember me writing about the wonderful colour variations seen in some aphid species and how this could be modified by their symbionts. In another twist, it seems that ants may have a say in this too, albeit at a colony level rather than at the clonal level.  The improbably named Mugwort aphid, Macrosiphoniella yomogicola  which is obligately ant-attended by the ant L. japonicus, is found in  colonies that are typically 65% green 35% red (Watanabe et al. 2016).  The question Watanabe and his colleagues asked is why do ants like this colour balance? One possibility is that red and green aphids have slightly different effects on the mugwort plants where they feed. Though green aphids produce more honeydew, red aphids seem to prevent the mugwort from flowering. Given that aphid colonies on a flowering mugwort go extinct, ants looking to maintain an aphid herd for more than a year might see an advantage to keeping reds around to guarantee a long-term food supply from their green sisters.

Aren’t insects wonderful?

 

References

Addicott, J.F. (1978) Competition for mutualists: aphids and ants.  Canadian Journal of Zoology, 56, 2093-2096.

Carroll, C.R. & Janzen, D.H. (1973) Ecology of foraging by ants.  Annual Review of Ecology & Systematics, 4, 231-257

Collins, C.M. & Leather, S.R. (2002) Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality?  Ecological Entomology, 27, 238-241.

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

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

El-Ziady, S. & Kenendy, J.S. (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli.  Proceedings of the Royal Entomological Society London (A), 31, 61-65

Endo, S. & Itino, T. (2012) The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons.  Research on Population Ecology, 54, 405-410.

Endo, S. & Itino, T. (2013) Myrmecophilus aphids produce cuticular hydrocarbons that resemble those of their tending ants.  Population Ecology, 55, 27-34.

Fischer, C.Y., Vanderplanck, M., Lognay, G.C., Detrain, C. & Verheggen, F.J. (2015a) Do aphids actively search for ant partner?  Insect Science, 22, 283-288.

Fischer, C.Y., Lognay, G.C., Detrain, C., Heil, M., Sabri, A., Thonart, P., Haubruge, E., & Verheggen, F.J. (2015) Bacteria may enhance species-association in an ant-aphid mutualistic relationship. Chemoecology, 25, 223-232.

Goidanich, A.  (1959) Le migrazioni coatte mirmecogene dello Stomaphis quercus Linnaeus, afido olociciclio monoico omotopo. Bollettino dell’Istituto di Entomologia della Università degli Studi di Bologna, 23, 93-131.

Goedart, J. & Lister, M. (1685) De Insectis, in Methodum Redactus; cum Notularum Additione. [Metamorphosis Naturalis] Smith, London.

Heie, O. (1980)  The Aphdioidea (Hemiptera) of Fennoscandia and Denmark. 1. Fauna Entomologica Scandinavica 9.Scandinavian Science Press, Klampenborg, Denmark.

Hough, W.S (1922) Observations on two mealy bugs Trionymus tritolii Forbes and Pseudococcus maritimus Ehrh. Entomologist’s News, 33, 1 7 1-76.

Hopkins, G.W. & Thacker, J.I. (1999) Ants and habitat specificity in aphids. Journal of Insect Conservation, 3, 25-31.

Jones, C.R. (1927) Ants and Their Relation to Aphids.  PhD Thesis, Iowa State College, USA.

Mittler, T.E. (1958a) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae).  II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew.  Journal of Experimental Biology, 35, 74-84.

Mueller, T.F., Blommers, L.H.M. & Mols, P.J.M. (1992) Woolly apple aphid (Eriosoma lanigerum Hausm., Hom., Aphidae) parasitism by Aphelinus mali Hal. (Hym., Aphelinidae) in relation to host stage and host colony size, shape and location.  Journal of Applied Entomology, 114, 143-154.

Oliver, T.H., Leather, S.R. & Cook, J.M. (2008)  Macroevolutionary patterns in the origin of mutualisms,  Journal of Evolutionary Biology, 21, 1597-1608.

Pontin, A.J. (1958)  A preliminary note on the eating of aphids by ants of the genus Lasius. Entomologist’s Monthly Magazine, 94, 9-11.

Pontin, A.J. (1960)  Some records of predators and parasites adapted to attack aphids attended by ants.  Entomologist’s Monthly Magazine, 95, 154-155.

Pontin, A.J. (1960)  Observations on the keeping of aphid eggs by ants of the genus Lasius.  Entomologist’s Monthly Magazine, 96, 198-199.

Pontin, A.J. (1978) The numbers and distributions of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecological Entomology, 3, 203-207.

Sakata, H. (1994) How an ant decides to prey on or to attend aphids.  Research on Population Ecology, 36, 45-51.

Sakata, H. (1995) Density-dependent predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attendant aphids Lachnus tropicalis and Myzocallis kuricola (Homoptera: Aphidae). Research on Population Ecology, 37, 159-164.

Skinner, G.J. & Whittaker, J.B. (1981) An Experimental investigation of inter-relationships between the wood-ant (Formica rufa) and some tree-canopy herbivores.  Journal of Applied Ecology, 50, 313-326.

Stadler, B. & Dixon, A.F.G. (1999)  Ant attendance in aphids: why different degrees of myrmecophily? Ecological Entomology, 24, 363-369.

Van Bruyssel, E. (1870) The Population of an Old Pear Tree.  MacMillan & Co, London

Vilagra, C.A., Ramirez, C.C. & Niemeyer, H.M. (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state.  Animal Behaviour, 64, 677-683.

Watanabe, S., Murakami, T., Yoshimura, J. & Hasegawa, E. (2016) Color piolymorphism in an aphid is maintained by attending ants.  Science Advances, 2, e1600606

Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera.  Annual Review of Entomology, 3, 307-344.

*in my opinion at any rate 🙂

**I have had to take this on faith as have not been able to get hold of the original reference and read it myself

***Trophobiosis is a symbiotic association between organisms where food is obtained or provided. The provider of food in the association is referred to as a trophobiont. The name is derived from the Greek τροφή trophē, meaning “nourishment” and -βίωσις -biosis which is short for the English symbiosis

****Perhaps they are too big for ants to mess with?  They are, however, very often surrounded by Vespid wasps who do appreciate the huge amount of honeydew deposited on the willow leaves and stems.

***** He must have enjoyed it because he also did his MSc project with me the following year 🙂

 

Post script

I began this post with an illustration from Van Bruyssel.  I finish it with this illustration from another early attempt to get children interested in entomology.  Unfortunately in this case the  ant attended aphids are the very opposite of what they should look like and he further compounds his error by telling his youthful audience that the aphids milk the aphids via their siphunculi 😦

The very opposite of what an ant-attend aphid looks like – from Half hours in the tiny world; wonders of insect life by C.F. Holder (1905)

Not all aphids have the same internal biomes

Headline message for those of you too busy to read the whole thing

Aphids have mutualistic symbiotic bacteria living inside them, one set, the primary endosymbionts, Buchnera aphidicola are obligate, i.e. in normal circumstances, the aphid can’t live without them and vice versa. All aphids have them. The others, the secondary symbionts, of which there are, at the last count, more than seven different species, are facultative, i.e. aphids can survive without them and not all aphids have them or the same combination of them. These can help the aphid in many ways, such as, making them more resistant to parasitic wasps, able to survive heat stress better and helping them use their host plants more efficiently. Hosting the secondary symbionts may, however, impose costs on the aphids.

Now read on, or if you have had enough of the story get back to work  🙂

Like us, aphids have a thriving internal ecology, they are inhabited by a number of bacteria or bacteria like organisms. The existence of these fellow travellers and the fact that they are transmitted transovarially, has been known for over a hundred years (Huxley, 1858; Peklo, 1912)*, although their role within the body of the aphids was not entirely understood for some time, despite Peklo’s conviction that they were symbionts and transferred via the eggs to the next generation. Some years later the Hungarian entomologist László Tóth** hypothesised that aphids because the plant sap that they feed on did not contain enough proteins to meet their demands for growth, must be obtaining the extra nitrogen they needed from their symbionts, although he was unable to prove this empirically (Tóth, 1940). This was very firmly disputed by Tom Mittler some years later, who using the giant willow aphid, Tuberolachnus salignus, showed that aphid honeydew and willow phloem sap contained the same amino acids (Mittler, 1953, 1958ab). It was not only aphidologists who were arguing about the nature and role of insect symbionts, as this extract from a review of the time makes clear,

“It is not our purpose here to harangue on terminology; suffice it to say that we will use “symbiote” for the microorganism and “host” for the larger organism (insect) involved in a mutualistic or seemingly mutualistic association.” (Richards & Brooks, 1958).

Interestingly it is in this paper that they mention, using the term “provocactive” the use of antibiotics to create aposymbiotic individuals in attempts to prove that the symbionts were first bacteria, and second, benefiting their insect hosts. The concluded that there was enough evidence to suggest that the endosymbionts were involved in some way in the nutritional and possibly reproductive processes of the insects studied, mainly cockroaches. At the time of the review no similar work had been done on aphids. A few years later though, two American entomologists sprayed aphids with several different antibiotics and found that this caused increased mortality and reduced fecundity when compared with untreated ones (Harries & Mattson, 1963). Presaging its future dominance in aphid symbiont work, one of the aphids was the pea aphid, Acyrthosiphon pisum. Antibiotics were also shown to eliminate and damage the symbionts associated with Aphis fabae followed by impaired development and fecundity in the aphid itself adding yet more evidence that the symbionts were an essential part of the aphid biome (Ehrhardt & Schmutterer, 1966). There was, however, still much debate as to how the symbionts provided proteins to the aphids, and although light and electron microscopy studies confirmed that the symbionts were definitely micro-organisms (Lamb & Hinde, 1967; Hinde, 1971), the answer to that question was to remain unanswered until the 1980s although the development of aphid artificial diets (Dadd & Krieger, 1967) which could be used in conjunction with antibiotic treatments, meant that it was possible to show that the symbionts provided the aphids with essential amino acids (Dadd & Kreiger, 1968; Mittler, 1971ab).*** Although the existence of secondary symbionts in other Homoptera was known (Buchner, 1965), it was not until Rosalind Hinde described them from the rose aphid, Macrosiphum rosae, that their presence in aphids was confirmed (Hinde, 1971).   Of course it was inevitable that they would then be discovered in the pea aphid although their role was unknown (Grifiths & Beck, 1973). Shortly afterwards they were able to show that material produced from the symbionts was passed into the body of the aphid (Griffiths & Beck, 1975) and it was also suggested suggested that it was possible that the primary symbionts were able to synthesise amino acids (Srivastava & Auclair, 1975) and sterols (Houk et al., 1976) for the benefit of their aphid hosts (partners). By the early 1980s it was accepted dogma that aphids were unable to reproduce or survive without their primary symbionts (Houk & Griffiths, 1980; Ishikawa, 1982) and by the late 1980s that dietary sterols were provided by the primary symbionts (Douglas, 1988).

Primary symbiont (P) in process of dividing seen next to secondary symbionts (S) and mitochondrion (m) from Houk & Griffiths (1980).

Despite the huge amount of research and the general acceptance that the endosymbionts were an integral part of the aphid’s biome “The mycetocyte symbionts are transmitted directly from one insect generation to the next through the female. There are no known cases of insects that acquire mycetocyte symbionts from the environment or from insects other than their parents” (Douglas , 1989), their putative identity was not determined until 1991 (Munson et al., 1991), when they were named Buchnera aphidicola, and incidentally placed in a brand new genus. Note however, that like some aphids, B. aphidicola represents a complex of closely related bacteria and not a single species (Moran & Baumann, 1994). Research on the role of the primary symbionts now picked up pace and it was soon confirmed that they were responsible for the synthesis of essential amino acids used by the aphids, such as tryptophan (Sasaki et al., 1991; Douglas & Prosser, 1992) and that it was definitely an obligate relationship on both sides**** (Moran & Baumann, 1994).

Now that the mystery of the obligate primary endosymbionts was ‘solved’, attention turned to the presumably facultative secondary symbionts, first noticed more than twenty years earlier (Hinde, 1971)***** began to be scrutinised in earnest. Nancy Moran and colleagues (Moran et al., 2005) identified three ‘species’ of secondary bacterial symbionts, Serratia symbiotica, Hamiltonella defensa and Regiella insecticola. As these are not found in all individuals of a species they are facultative rather than obligate. The secondary symbionts were soon shown not to have nutritional benefits for the aphids (Douglas et al., 2006). They are instead linked to a whole swathe of aphid life history attributes, ranging from resistance to parasitoids (Oliver et al., 2003; 2005; Schmid et al., 2012), resistance to heat and other abiotic stressors (Montllor et al., 2002; Russell & Moran 2006; Enders & Miller, 2016) and to host plant use (Tsuchida et al., 2004; McLean et al., 2011; Zytynska et al., 2016).

And finally, Mittler (1971b) mentions the reddish colouration developed by aphids reared on some of the antibiotic diets and hypothesises that this may be linked to the symbionts. I have written earlier about aphid colour variants and the possibility that the symbionts may have something to do with it. The grain aphid, Sitobion avenae has a number of colour variants and it was suggested that levels of carotenoids present might have something to do with the colours expressed and that in some way this was controlled by the presence of absence of symbionts (Jenkins et al., 1999). More recently Tsuchida and colleagues in a series of elegant experiments on the ubiquitous pea aphid, have shown that the intensity of green colouration is dependent on the presence of yet another endosymbiont, a Rickettsiella (Tsuchida et al., 2010). The authors hypothesise that being green

Elegant demonstration that in some strains of the pea aphid, green colour is a sign of an infection by Rickettsiella (Tsuchida et al., 2010).

rather than pink or red, may reduce predation by ladybirds as has been suggested before (Losey et al., 1997).

New secondary symbionts continue to be discovered and with each discovery, new hypotheses are raised and tested. It would seem that there is a whole ecology of secondary symbionts within the aphid biome waiting to be explored and written about (Zytynska & Weisser, 2016). What are you waiting for, but do remember to come up for air sometime and relate what you find back to the ecology of the aphids 🙂

 

References

Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York.

Dadd, R.H. & Krieger, D.L. (1967) Continuous rearing of aphids of the Aphis fabae complex on sterile synthetic diet. Journal of Economic Entomology, 60, 1512-1514.

Dadd, R.H. & Krieger, D.L. (1968) Dietary amino acid requirements of the aphid Myzus persicae. Journal of Insect Physiology, 14, 741-764.

Douglas, A.E. (1988) On the source of sterols in the green peach aphid, Myzus persicae, reared on holidic diets. Journal of Insect Physiology, 34, 403-408.

Douglas, A.E. (1998) Mycetocyte symbiosis in insects. Biological Reviews, 64, 409-434.

Douglas, A.E. & Prosser, W.A. (1992) Sythesis of the essential amiono acid trypthotan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38, 565-568.

Douglas, A.E., Francois, C.M.L.J. & Minto, L.B. (2006) Facultative ‘secondary’ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiological Entomology, 31, 262-269.

Ehrhardt, P. & Schmutterer, H. (1966) Die Wirkung Verschiedener Antibiotica auf Entwicklung und Symbionten Künstlich Ernährter Bohnenblattläuse (Aphis fabae Scop.). Zeitschrift für Morphologie und Ökologie der Tiere, 56, 1-20.

Enders, L.S. & Miller, N.J. (2016)Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid. Ecology & Evolution, 6, 818-829.

Griffiths, G.W. & Beck, S.D. (1973) Intracellular symbiotes of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 19, 75-84.

Griffiths, G.W. & Beck, S.D. (1975) Ultrastructure of pea aphid mycetocystes: evidence for symbiote secretion. Cell & Tissue Research, 159, 351-367.

Harries, F.H. & Mattson, V.J. (1963) Effects of some antibiotics on three aphid species. Journal of Economic Entomology, 56, 412-414.

Hinde, R. (1971) The control of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. Journal of Insect Physiology, 17, 1791-1800.

Houk, E.J. & Griffiths, G.W. (1980) Intracellular symbiotes of the Homoptera. Annual Review of Entomology, 25, 161-187.

Houk, E.J., Griffiths, G.W. & Beck, S.D. (1976) Lipid metabolism in the symbiotes of the pea aphid, Acyrthosiphon pisum. Comparative Biochemistry & Physiology, 54B, 427-431.

Huxley, T.H. (1858) On the agamic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society of London, 22, 193-219.

Ishikawa, H. (1978) Intracellular symbionts as a major source of the ribosomal RNAs in the aphid mycetocytes. Biochemical & Biophysical Research Communications, 81, 993-999.

Ishikawa, H. (1982) Isolation of the intracellular symbionts and partial characterizations of their RNA species of the elder aphid, Acyrthosiphon magnoliae. Comparative Biochemistry & Physiology, 72B, 239-247.

Jenkins,  R.L., Loxdale, H.D., Brookes, C.P. & Dixon, A.F.G. (1999)  The major carotenoid pigments of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae).  Physiological Entomology, 24, 171-178. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-3032.1999.00128.x/pdf

Lamb, R.J. & Hinde, R. (1967) Structure and development of the mycetome in the cabbage aphid, Brevicoryne brassciae. Journal of invertebrate Pathology, 9, 3-11.

Losey, J. E., Ives, A. R., Harmon, J., Ballantyne, F. &Brown, C. (1997). A polymorphism maintained by opposite patterns of parasitism and predation. Nature, 388, 269-272.

McLean, A.H.C., van Asch, M., Ferrari, J. & Godfray, H.C.J. (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B., 278, 760-766.

Mittler, T.E. (1953) Amino-acids in phloem sap and their excretion by aphids. Nature, 172, 207.

Mittler, T.E. (1958a) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. Journal of Experimental Biology, 35, 74-84.

Mittler, T.E. (1958b) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). III The nitrogen economy. Journal of Experimental Biology, 35, 626-638.

Mittler, T.E. (1971a) Dietary amino acid requirements of the aphid Myzus persicae affected by antibiotic uptake. Journal of Nutrition, 101, 1023-1028.

Mittler, T.E. (1971b) Some effects on the aphid Myzus persicae of ingesting antibiotics incorporated into artificial diets. Journal of Insect Physiology, 17, 1333-1347.

Montllor, C.B., Maxmen, A. & Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea pahids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.

Moran, N. & Baumann, P. (1994) Phylogenetics of cytoplasmically inherited microrganisms of arthropods. Trends in Ecology & Evolution, 9, 15-20.

Moran, N.A., Russell, J.A., Koga, R. & Fukatsu, T. (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied & Environmental Microbiology, 71, 3302-3310.

Munson, M.A., Baumann, P. & Kinsey, M.G. (1991) Buchnera gen. nov. and Buchnera aphidicola sp. Nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. International Journal of Systematic Bacteriology, 41, 566-568.

Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences USA, 100, 1803-1807.

Oliver, K.M., Moran, N.A. & Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences USA, 102, 12795-12800.

Peklo, J (1912) Über symbiotische Bakterien der Aphiden. Berichte der Deutschen Botanischen Gesellschaft, 30, 416-419.

Richards, A.G. & Brooks, M.A. (1958) Internal symbiosis in insects. Annual Review of Entomology, 3, 37-56.

Russell, J.A. & Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B, 273, 603-610.

Sasaki, T., Hayashi, H. & Ishikawa, H. (1991) Growth and reproduction of the symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum mainatained on artificial diets. Journal of Insect Physiology, 37, 749-756.

Schmid, M., Sieber, R., Zimmermann, Y.S. & Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26, 207-215.

Srivastava P.N. & Auclair, J.L. (1975) Role of single amino acids in phagostimualtion, growth, and survival of Acyrthosiphon pisum. Journal of Insect Physiology, 21, 1865-1871.

Tóth, L. (1940) The protein metabolism of aphids. Annales Musei Nationalis Hungarici 33, 167-171.

Tsuchida, T., Koga, R. & Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989.

Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., Simon, J. C. &Fukatsu, T. (2010). Symbiotic bacterium modifies aphid body color. Science 330: 1102-1104.

Zytynska, S. E. &Weisser, W. W. (2016). The natural occurrence of secondary bacterial symbionts in aphids. Ecological Entomology, 41, 13-26.

Zytynska, S.E., Meyer, S.T., Sturm, S., Ullmann, W., Mehrparvar, M. & Weisser, W.W. (2016) Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia, 180, 735-747.

 

Footnotes

*I should point out that although Huxley clearly described the structure and contents of the mycetocytes he had absolutely no idea what they were and what function, if any, they had. Despite the many authors who supported Peklo’s claim that the contents of the mycetocytes were bacteria he was still having to defend himself against detractors more than 50 years later (Peklo, 1953).

Peklo, J. (1953) Microorganisms or mitochondria? Science, 118, 202-206.

 

**not to be confused with the László Tóth who vandalised Michelangelo’s Pietà

***interestingly, although the existence of primary symbionts in aphids and their possible role in aphid nutrition was by then firmly established, my vade mecum as a student, Tony Dixon’s Biology of Aphids, makes no mention of them at all, although first published in 1973. The first edition of Aphid Ecology (1985) also by Tony Dixon, only devotes three quarters of a page to them, but by the second edition, published in 1998, they get a whole chapter to themselves.

Buchnera appears to have been ‘lost’ but replaced by a yeast like symbiont (Braendle et al., (2003).

Braendle, C., Miura, T., Bickel, R., Shingleton, A.W., Kambhampari, S. & Stern, D.L. (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PloS Biology, 1, e21. doi:10.1371/journal.pbio.0000021.

 

*****although Huxley’s description of the unknown structures that he saw in aphids in 1858, does seem to include secondary symbionts as well as the primary ones.

Not all aphids get lost

Although aphids are very good at kicking, we know that aphids would not be very good at football as they are very short-sighted (Doring et al., 2008) but does that mean that they are not very good at finding their host plants? There is a common misperception, and not just confined to non-entomologists, that aphids are no more than aerial plankton. In 1924 Charles Elton

whilst on an expedition to Nordaustlandet* (the second largest of the Spitsbergen group and almost entirely covered by ice) reported finding large numbers of aphids, many still alive, later identified as Dilachnus piceae (now known as Cinara piceae) (Elton, 1925).

Cinara piceae the Greater Black Spruce Aphid –big and beautiful.

 

He suggested that the aphids came from the Kola Peninsula, a distance of about 800 miles (almost 1300 km) due to the strong south and south-east winds blowing at the time. He estimated that they would have made the journey within twelve to twenty-four hours. This was regarded as being an example of totally passive migration and used as one of many examples of aerial plankton** (Gislen, 1948). This is, however, probably not giving aphids credit for what they are capable of doing when it comes to flight. Berry & Taylor (1968), who sampled aphids at 610 m above the grounds using aeroplanes, implied that the aphids, although using jet streams, were flying rather than floating (page 718 and page 720) and that they would descend to the ground in the evening and not fly during the night.

Aphids don’t usually fly during the night. (From Berry & Taylor (1968)).

Dixon (1971) interprets this somewhat differently and suggests that the “movement of the air in which it is flying determines the direction of its flight and the distance it will travel” but then goes on to say “after flying for an hour or two aphids settle indiscriminately on plants”. So yes the speed of the air in which the aphid is flying will determine how far it flies in a set time, but as aphids can fly much longer than an hour or two, active flights of from between 7-12 hours have been recorded (Cockbain, 1961), this rather suggests that the aphids are making a “decision” to stop flying and descend from the jet stream. That said, in the words of the great C.G. Johnson “aphids are weak flyers”, they cannot make progress against headwinds of more than 2 km per hour (Johnson, 1954), although Trevor Lewis gives them slightly more power and suggests that the can navigate against winds of up to 3 km per hour (Lewis, 1964).

Whatever the upper limit is, it doesn’t mean that they are powerless when it comes to ‘deciding’ when to stop flying. In the words of Hugh Loxdale and colleagues, “aphids are not passive objects” (Loxdale et al, 1993). Aphidologists, were until the 1980s (Kennedy, 1986), generally somewhat sceptical about the ability of aphids to direct their flight in relation to specific host finding from the air and not just flying towards plants of the right colour (Kennedy et al., 1961), or at all after take-off (Haine, 1955). The general consensus now, is that aphids control the direction of their flight in the boundary layer*** but that it is determined by the wind at higher altitudes (Loxdale et al., 1993).   Whilst we are discussing viewpoints, another point of debate is on whether aphids migrate or not. Loxdale et al., (1993) state that “migration can be viewed ecologically as population redistribution through movement, regardless of whether deliberate of uncontrolled or from the behavioural viewpoint of a persistent straightened-out movement affected by the animal’s own locomotory exertions or by its active embarkation on a vehicle”. In the case of aphids the vehicle could be the wind. Under both definitions, aphids can be defined as undertaking migrations. Long-distance migration by aphids is defined as being greater than 20 km and short-distance (local) migration being less than this (Loxdale et al., 1993). Long-distance migration is likely to be the exception rather than the rule with most aphids making local flights and not venturing out of the boundary layer, sometimes travelling distances no more than a few hundred metres (Loxdale et al., 1993).

There are different types of winged aphids (morphs) and these show different angles of take-off and rates of climb.  In Aphis fabae for example, which host –alternates between spindle and bean, the gynoparae which migrate from the secondary host to the primary host, have a steeper angle of take-off and climb more rapidly than the alate exules which only disperse between the secondary host plants (David & Hardie, 1988).

http://influentialpoints.com/Images/Rhopalosiphum_padi_emigrant_alate_departing_from_primary_host_c2013-05-21_11-25-12ew.jpg

The gynoparae are thus much more likely to end up in the jet stream and be carried longer distances, with, of course, a greater chance of getting lost (Ward et al., 1998). The alate exules however, may only land in the next field or even in the same one, and easily find a new host plant (Loxdale et al., 1993). These differences between the morphs of host alternating aphids are also seen in the bird cherry-oat aphid Rhopalosiphum padi (Nottingham et al., 1991).  Once safely air-borne, the aphids then have another set of problems to overcome.

How do they ‘decide’ when to land? How do they ‘know’ that there are host plants below them? Aphids have two main senses that help them locate their host plants, vision and smell (odour recognition) (Kring, 1972; Döring, 2014). Generally speaking, aphids respond positively to what we perceive as green or yellow light and negatively to blue and red light (Döring & Chittka, 2007) although this is not an absolute rule. Some aphids are known to preferentially choose yellowing leaves (sign of previous infestation) e.g. Black Pecan Aphid Melanocallis caryaefoliae (Cottrell et al., 2009) which indicates a pretty sophisticated host finding suite of behaviours. Aphids in flight chambers will delay landing if presented with non-host odours even in the presence of a green target (Nottingham & Hardie, 1993) and conversely can be attracted to colourless water traps that have been scented with host plant odours (Chapman et al., 1981). Aphids are thus using both visual and olfactory cues to locate their host plants and to ‘decide’ when to descend from the jet stream or boundary layer (Kring, 1972; Döring, 2014). They are not merely aerial plankton, nor are they entirely at the mercy of the winds, they do not deserve to be described as passive (Reynolds & Reynolds, 2009).

Once at ground level and on a potential host plant, aphids go through a complicated suite of behaviours to determine if the host is suitable or not; if the plant meets all the required

From air to plant – how aphids chose their host plants – after Dixon (1973).

 

criteria, then the aphid will start feeding and reproducing. It is interesting to note that although there may be a lot of aphids in the air, the number of plants on the ground that

Settled safely and producing babies 🙂

http://beyondthehumaneye.blogspot.co.uk/2012/06/aphids.html  https://simonleather.files.wordpress.com/2016/04/cd0a4-aphidbirth2small.jpg

 

are infested with them is relatively low, about 10% in a diverse landscape (Staab et al., 2015), although in a crop, the level of infestation can approach 100% (e.g. Carter et al., 1980). The fact that in some cases less than 1% of those that set off will have found a host plant (Ward et al., 1998) is not a problem when you are a member of clone; as long as not all of the members of a clone gets lost the journey has been a success.

They may be small, they may be weak flyers, but enough of them find a suitable host plant to keep the clone alive and kicking; not all aphids get lost.

 

References

Carter, N., Mclean, I.F.G., Watt, A.D., & Dixon, A.F.G. (1980) Cereal aphids – a case study and review. Applied Biology, 5, 271-348.

Chapman, R.F., Bernays, E.A., & Simpson, S.J. (1981) Attraction and repulsion of the aphid, Cavariella aegopodii, by plant odors. Journal of Chemical Ecology, 7, 881-888.

Cockbain, A.J. (1961) Fuel utilization and duration of tethered flight in Aphis fabae Scop. Journal of Experimental Biology, 38, 163-174.

Cottrell, T.E., Wood, B.W. & Xinzhi, N. (2009) Chlorotic feeding injury by the Black Pecan Aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environmental Entomology, 38, 411-416

David, C.T. & Hardie, J. (1988) The visual responses of free-flying summer and autumn forms of the black bean aphid, Aphis fabae, in an automated flight chamber. Physiological Entomology, 13, 277-284.

Dixon, A.F.G. (1971) Migration in aphids. Science Progress, Oxford, 59, 41-53.

Dixon, A.F.G. (1973) Biology of Aphids, Edward Arnold, London.

Döring, T.F. & Chittka, L. (2007) Visual ecology of aphids – a classcial review on the role of colours in host finding. Arthropod-Plant Interactions, 1, 3-16.

Döring, T., Hardie, J., Leather, S.R., Spaethe, J., & Chittka, L. (2008) Can aphids play football? Antenna, 32, 146-147.

Döring, T. (2014) How aphids find their host plants, how they don’t. Annals of Applied Biology, 165, 3-26.

Elton, C.S. (1925) The dispersal of insects to Spitsbergen. Transactions of the Entomological Society of London, 73, 289-299.

Gislen, T. (1948) Aerial plankton and its conditions of life. Biological Reviews, 23, 109-126.

Haine, E. (1955) Aphid take-off in controlled wind speeds. Nature, 175, 474-475

Johnson, C.G. (1951) The study of wind-borne insect populations in relation to terrestrial ecology, flight periodicity and the estimation of aerial populations. Science Progress, 39, 41-62.

Johnson, C.G. (1954) Aphid migration in relation to weather. Biological Reviews, 29, 87-118

Kennedy, J. S., Booth, C. O. & Kershaw, W. J. S. (1961). Host finding by aphids in the field III Visual attraction. Annals of Applied Biology, 49, 1-21.

Kring, J.B. (1972) Flight behavior of aphids. Annual Review of Entomology, 17, 461-492.

Lewis, T. (1964) The effects of shelter on the distribution of insect pests. Scientific Horticulture, 17, 74-84

Loxdale, H. D., Hardie, J., Halbert, S., Foottit, R., Kidd, N. A. C. &Carter, C. I. (1993).The relative importance of short-range and long-range movement of flying aphids. Biological Reviews of the Cambridge Philosophical Society, 68, 291-312.

Nottingham, S.F., Hardie, J. & Tatchell, G.M. (1991) Flight behaviour of the bird cherry aphid, Rhopalosiphum padi. Physiological Entomology, 16, 223-229.

Reynolds, A.M. & Reynolds, D.R. (2009)  Aphid aerial desnsity profiles are consistent with turbulent advection amplifying flight behaviours: abandoning the epithet ‘passive’. Proceedings of the Royal Society B, 276, 137-143.

Staab, M., Blüthgen, N., & Klein, A.M. (2015) Tree diversity alters the structure of a tri-trophic network in a biodiversity experiment Oikos, 124, 827-834.

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.

 

Post script

Political and geographic borders are not factors that deter aphid migrants, Wiktelius (1984) points out that aphids regularly make the journey across the Baltic in both directions to and from Sweden.

Wiktelius, S. (1984) Long range migration of aphids into Sweden. International Journal of Biometeorology, 28, 185-200.

 

*Elton refers to it as North-East Land

** Johnson (1951) objects to this terminology in no uncertain terms. That said, as there are records of non-winged aphids being caught by aircraft (Kring, 1972), it does suggest that there may be some accidental migration going on.

*** The UK Met Office defines the boundary layer as “that part of the atmosphere that directly feels the effect of the earth’s surface” and goes on to say that depending on local conditions it can range in depth from a few metres to several kilometres.

Not all books about aphids are for grown-ups!

A couple of weeks ago I was preparing a new lecture on the endocrine control of alary polymorphism in aphids. As is my wont when I want to get myself in the right frame of mind for aphid lecture writing, I went across to my book shelf to get down my copy of Tony Dixon’s excellent little book The Biology of Aphids (it might be old but it has some of the simplest and clearest explanations of complex aphid biology that I know of).

To my horror (and shock) it wasn’t here.  I had obviously lent it to a student and not instilled the fear of death into them 🙂  Once I got over my shock I turned to the internet (Amazon to be exact), and searched for an acceptable copy, which I successfully found*.  Whilst browsing the virtual shelves however, my eye was caught by a book with the intriguing title Anna Aphid.    I was stunned and amused, and as it cost less than a fiver including postage, I added it to my virtual basket.

A few days later it arrive and I was the proud owner of Anna Aphid  by Christine Goppel.

Anna Aphid – http://www.christinegoppel.de/flashseite.html

I instantly sat down and read it cover to cover (it isn’t very long). I don’t usually post book reviews, but having read it and pedantically groaned at the aphidological errors, I thought I might as well as share my thoughts with you all.  Anna Aphid was published by North-South Books in September  2005, and if they had any in stock you could buy it new for £9.99, (or $8.45 in the USA); don’t worry, there are plenty of used copies available, and mine was in very good condition.

The blurb for states “A tiny aphid named Anna lives on a big green leaf with her family. But Anna is different from the other aphids. She is curious to discover what lies beyond their green world. So Anna sets off to explore. In an entertaining visual guessing game, we see things from Anna’s point of view”

This is a fairly accurate statement of the content, although it gives things away a bit by saying that she lives on a leaf, as in the book Anna thinks she is living on a planet (remove the letter e and you get the pun).  The book which is very well-written, details the adventures of Anna from her beginnings as an apterous (non-winged) aphid, living with her family, including her father, (yes, a big aphidological blooper).  She expresses a wish to see the rest of the universe, and despite everything I had just read about endocrine control of alary polymorphism 🙂 suddenly sprouts wings, although given that her living conditions as shown in the illustrations seem quite crowded, this would be acceptable if she had just moulted to adulthood.  As an aphid pedant, I couldn’t help noticing that she only had one pair of wings instead of the normal two that I would expect.  The cephalo-thorax-abdomen body structure was also hard to ignore, as was the fact that poor Anna seemed to have mislaid a pair of legs somewhere.

Anna takes flight (she looks more like a frog with wings than an aphid)

Having taken flight and set off into the unknown vastness of space (from an aphid’s point of view), Anna has a series of adventures and near escapes from death.  She flies too near to the sun, narrowly escaping being burnt to a cinder, then lands on the moon where she attempts

Anna landing on the moon and giving us an interesting view of aphid feet!

to eat the strange vegetation she finds there , in the course of which she reveals that instead of having piercing and sucking mouthparts, she appears to be equipped with chewing ones.

Anna exhibiting non-standard mouth parts as she eats moon fodder.

Anna then hitches a lift on a comet, and lands on a shaggy red planet, which turns out to be yet another dangerous place as she is almost sucked into a black hole. Luckily, an exploding planet hurls Anna into a bubbling sea where she only just escapes drowning by climbing onto a small island.

The bubbling sea

 Safe from drowning, a gentle warm breeze helps her recover her strength enabling her to fly back to her home planet, and an excited

A warm breeze sending Anna safely on her way home

welcome from her whole family. She reports back to her father “I didn’t meet any other forms of intelligent life, but the universe is so big! Who knows what is out there”  Taken as an analogy for the huge number of insects that remain to be discovered, classified and researched, I can only agree with her sentiments.

The universe revealed! Can you guess which objects were which planetary features?

Actually, pedantic aphidological quibbles aside, I quite enjoyed the book.  It was a very pleasant surprise to find aphids featuring in such a positive and amusing way in fiction.  It would have been nice if the biology, especially the mouth parts, eyes, and other anatomical features were a bit more true to life, but it is just possible that I am slightly jealous that it had never occurred to me to write a story about an aphid 🙂  If you have children, grand-children, nieces or nephews of a suitable age I would certainly recommend it as a very suitable present and hopefully having read it, or had it read to them, they will learn to love aphids as much as I do.

 

References

Dixon, A.F.G. (1973) The Biology of Aphids, Edward Arnold, London

 

Post script

*I actually bought two copies of The Biology of Aphids, one which was in less good condition.  The sale details included the phrase “having owner’s name on inside front cover”, so I had to buy it just to check that it wasn’t my original copy that had been sold on by whichever student had ‘borrowed’ it.  As I should have expected it wasn’t mine 🙂 but still, it is always handy to have a spare copy in case one goes walkabout like my original did.

 

Post post script

In one of my emails to my daughter who lives in Australia, I mentioned that I had bought Anna Aphid and to my surprise received the following reply “I bought that book! The boys know about aphids, especially Toby; “ladybugs eat them” “so I was behind the curve yet again!

 

 

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

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

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

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

a suitably amusingly appropriate sign on the door.

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

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

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

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

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

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

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

 

Reference

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

 

Sensu stricto in the narrow sense; Sensu lato broadly speaking

 

A non-entomological post script

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

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

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

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

The Great Nijinsky – looking a bit fed-up?

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

Cancan dancer extraordinaire, La Goulue (The Glutton).

Robert Mayet – Inventor of the moped

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

Christmas will apparently soon be with us!

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

 

Mellow Yellow – Not all aphids live on green leaves

I have written before about aphids and how their quest for the ideal food plant may explain the evolution of host alternation; we find that most aphid species tend to be associated with rapidly growing meristems, or newly flushing leaves (Dixon, 2005). Some aphids are so keen on young plant tissue that they ‘engineer’ youth in their host plants, injecting salivary compounds and forming leaf–rolls, pseudo-galls and galls, all of which act as nutrient sinks and lengthen the time that the modified leaves stay green and nutrient-rich

 Leaf-roll caused by Rhopalosiphum padi on bird cherry, Prunus padus.

Pronounced leaf roll pseudo-gall caused by Myzus cerasi on Prunus avium.

Non host-alternating (autoecious) aphids, such as the sycamore aphid Drepanosiphum platanoidis, the maple aphid, Periphyllus testudinaceus, or the birch aphid, Euceraphis punctipennis, have no such escape route; they are confined to their tree host for the year, albeit, they can, if they ‘wish’, fly to another tree of the same species, but essentially they are held hostage by the their host plant. As the season progresses, leaf nutritional and physical properties change; going from young tender green leaves, with high nitrogen and water contents, to mature, tough leaves, low in nitrogen and water to yellow senescing leaves with again, higher nitrogen levels (Awmack & Leather, 2002) and finally of course, dead brown leaves of no nutritional value.

Sycamore and maple aphids, enter a state of suspended animation ‘summer aestivation’ (Essig, 1952; Dixon, 1963), whilst birch and poplar aphids, whose hosts plants often produce new growth during the year, ‘track’ these new leaves (Wratten, 1974; Gould et al., 2007). As far as these aphids are concerned young tissue is their best food source, with senescent tissue being second best and mature leaves being least favoured. During the summer they will, however, take advantage of mature leaves that are prematurely senescing, such as those attacked by leaf diseases such as tar spot. I have often found sycamore aphids feeding and reproducing on these infected leaves whilst those aphids on neighbouring mature leaves remain in aestivation.

Effects of tar spot on sycamore leaves

Host-alternating (heteroecious) aphids on the other hand are somewhat different. As their life cycle includes a programmed migration back to their primary tree host in autumn, those autumn morphs (oviparae) are adapted to senescent tissue (Leather & Dixon, 1982, Kundu & Dixon, 1993, 1994). Similarly, the spring morphs (fundatrices and fundatrigeniae) are adapted to young leaves and find it difficult or impossible, to make a living on senescent leaves.

There are yet other aphids, such as the green spruce aphid Elatobium abietinum, the pine aphid, Eulachnus agilis and the black pecan aphid, Melanocallis caryaefoliae, that are senescence specialists. In contrast to the flush specialists, these aphids engineer senescence, also using salivary compounds,  and are unable to survive on young foliage (Bliss, 1973; Fisher, 1987; Cottrell et al., 2009).

Elatobium abietinum ‘engineering’ senescence on spruce needles and avoiding young flushing tissue.

It is interesting to speculate that perhaps these tree-dwelling non host-alternating aphids are secondarily derived from the autumn part of the life-cycle of host-alternating aphids. After all, if non host-alternating aphids on herbaceous host plants are off-shoots of the summer part of the host-alternating life-cycle why not the other way round. There is just so much more to learn about aphids. Yet another reason why I love aphids so much 😉

References

Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817-844.

Bliss, M., Yendol, W.G., & Kearby, W.H. (1973) Probing behaviour of Eulachnus agilis and injury to Scotch pine. Journal of Economic Entomology, 66, 651-655.

Cottrell, T.E., Wood, B.W. & Ni, X. (2009) Chlorotic feeding injury by the Black Pecan Aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environmental Entomology, 38, 411-416.

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

Dixon, A.F.G. (2005) Insect Herbivore-Host Dynamics. Cambridge University Press, Cambridge.

Fisher, M. (1987) The effect of previously infested spruce needles on the growth of the green spruce aphid, Elatobium abietinum. Annals of Applied Biology, 111, 33-41.

Gould, G.G., Jones, C.G., Rifleman, P., Perez, A., & Coelman, J.S. (2007) Variation in Eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behaviour of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae). Environmental Entomology, 36, 1212-1225.

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. (1994) Feeding on their primary host by return migrants of the host alternating aphid, Cavariella aegopodii. Ecological Entomology, 19, 83-86.

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.

Wratten, S.D. (1974) Aggregation in the birch aphid, Euceraphis punctipennis (Zett.) in relation to food quality. Journal of Animal Ecology, 43, 191-198.

 

Post script

A lot of what I describe comes from a talk I gave in 2009 at a workshop in Oxford on autumn colours (the output of which was Archetti, M., Döring, T.F., Hagen, S.B., Hughes, N.M., Leather, S.R., Lee, D.W., Lev-Yadun, S., Manetas, Y., Ougham, H.J., Schaberg, P.G., & Thomas, H. (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends in Ecology & Evolution, 24, 166-173. I always meant to write the talk up as an Opinion piece but procrastination set in badly. I was somewhat annoyed with myself when earlier this year this excellent piece by the legendary ecologist and entomologist, Tom White, appeared; I have only myself to blame, six years is a very long bit of procrastination 😉

White, T.C.R. (2015) Senescence-feeders: a new trophic sub-guild of insect herbivores Journal of Applied Entomology, 139, 11-22.

 

Post post script

This post is dedicated to my eldest son, Sam, who died quietly in his sleep, at a tragically young age, December 23^rd 2010.   It would have been his birthday on the 21st May.  Despite being a molecular biologist, (he worked at the Sanger Institute), he was as green as you can get, a great naturalist and conservationist, with an incredibly gentle soul. He strongly believed in conserving the World’s natural resources and amused colleagues by sticking up signs in the toilets at the Sanger, which read “If its yellow let it mellow, if its brown flush it down”.

 

He is sorely missed by us all. He also had more Nature papers than me 😉

Parkhill, J., Achtman, M., James, K.D. et al., (2000) Complete DNA sequence of a serogroup A strain of Neisseria meningitides. Nature, 404, 502-506

Parkhill, J., Dougan, G. , James, K.D. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature, 413, 848-852.

Parkhill, J., Wren, B.W., Thomson, N.R. et al., (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523-527.

Parkhill, J., Sebaihia, M., Preston, A. et al., (2003) Comparative analysis of the genome sequences of Bordetella pertussis,   Bordetella parapertussis and Bordetella bronchiseptica. Nature Genetics, 35, 32-40

Wood, V., Gwilliam, R. Rajandream, M.A. et al., (2002) The genome sequence of Schizosaccharomyces pombe . Nature, 415, 871-880

 

 

Not all aphids take the same risks

In 1970 an entomologist working on the black bean aphid, Aphis fabae, at Rothamsted Experimental Station (as it then was),  noted that he could categorise the winged individuals as either migrants, flyers or non-flyers; the former flying before they reproduced, the second flying after they reproduced and the final category, never flying (Shaw, 1970).  To describe this phenomenon he used the phrase “migratory urge” a term previously only used in the ornithological literature.

A few years later a group of PhD students in Tony Dixon’s lab at the University of East Anglia started dissecting aphids and counting their ovarioles, finding that unlike most other insects, ovariole number was variable within a species and not related to adult weight (Dixon & Dharma, 1980; Wellings et al., 1980; Leather, 1983).  Generally speaking, in insects, including aphids, the heavier they are, the more fecund they are, although in some instances this is not always true (Leather, 1988).

Figure 1 taken from http://www.aphidsonworldsplants.info/Cloning_Experts_3.htm

Figure 2 What aphid ovarioles really look like Dombrovsky  et al. BMC Research Notes 2009 2:185   doi:10.1186/1756-0500-2-185

What we found then (Wellings et al., 1980), and later (Leather et al., 1988), was that aphids with wings (alatae) even those from the same clone, had much more variability in the number of ovarioles contained within them than those without wings (apterae) (Leather et al., 1988), and that the more ovarioles an aphid contained the more fecund it was, although as mentioned earlier the number of ovarioles appeared to be independent of weight (Leather & Wellings, 1981).

So what does this have to do with migratory urge in Aphis fabae? In the early 1980s Keith Walters was working on migration in cereal aphids (Sitobion avenae and Rhopalosiphum padi) and discovered, that as with Aphis fabae these two species also produced alatae with different flight attributes (Walters & Dixon, 1983).  Building on what we in our group had discovered about ovarioles, Keith was able to show that the degree of migratory urge in aphids was determined by the number of ovarioles they contained. The greater the number of ovarioles the more reluctant they were to take flight (Figure 3ab).

Figure 3a Relationship between number of ovarioles and time to take-off (minutes) in Sitobion avenae  (Drawn from data in Walters & Dixon, 1983).

Figure 3b Relationship between number of ovarioles and time to take-off (minutes) in Rhopaloisphum padi  (Drawn from data in Walters & Dixon, 1983).

 He also found that the fewer the number of ovarioles, the steeper the angle of take-off was (Figure 4) i.e. aphids with few ovarioles climbed faster and more steeply and were thus more likely to end  up higher in the air, and thus more likely to travel further than those

Figure 4 Relationship between number of ovarioles and angle of take-off (degrees) in Rhopalosiphum padi (drawn from data in Walters & Dixon, 1983).

taking off at a shallower angle.  He also showed that resistance to starvation was greater in those aphids with fewer ovarioles and that they could also fly for longer periods of time.  Given that alatae of Aphis fabae also have a variable number of ovarioles, 6-12 (Leather et al., 1988), we can see that this fits in very well with Shaw’s classification of migrants, flyers and non-flyers.

This is yet another great example of the flexibility (plasticity) of the aphid clone.  By producing offspring that have different flight capabilities and propensities, the clone is able to hedge its bets in times of adversity; alate aphids in many aphid species are produced in response to crowding and/or poor nutritional quality (Dixon, 1973).  This deterioration in living conditions could be very local i.e. restricted to the plant on which the aphid is feeding or its immediate neighbours, slightly more widespread, i.e. at a field scale or at a much more widespread landscape scale.  Given that long distance aphid migration is very costly (only a tiny proportion survive, Ward et al, 1998) the best option is to spread the risk between the members of your clone.  Those individuals with more ovarioles and greater potential fecundity make the low risk short-distance hops (trivial flights), but take the chance that the next door plant might be just as bad as the one left behind and also within easy reach of natural enemies, but with a higher chance of arriving and reproducing.

A risk taking aphid!

 

At the other end of the scale, those clone members with fewer ovarioles and reduced potential fecundity make the long distance migratory flights, with the risk of not finding a suitable host plant in time, but with the chance that if they do, it will be highly nutritious and natural enemy-free.  A really good example of not putting all your eggs in one basket and yet again a demonstration of what fantastic insects aphids are 😉

 

References

Dixon, A.F.G. (1973) Biology of Aphids Edward Arnold, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14.

Leather, S.R. (1983) Evidence of ovulation after adult moult in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 33, 348-349.

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. & Welllings, P.W. (1981) Ovariole number and fecundity in aphids. Entomologia experimentalis et applicata, 30, 128-133.

Leather, S.R., Wellings, P.W., & Walters, K.F.A. (1988) Variation in ovariole number within the Aphidoidea. Journal of Natural History, 22, 381-393.

Shaw, M.J.P. (1970) Effects of population density on the alienicolae of Aphis fabae Scop.II The effects of crowding on the expression of migratory urge among alatae in the laboratory. Annals of Applied Biology, 65, 197-203.

Walters, K.F.A. & Dixon, A.F.G. (1983) Migratory urge and reproductive investment in aphids: variation within clones. Oecologia, 58, 70-75.

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.

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

 

The Scent of Fear – the aphid alarm pheromone

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

 

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

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

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

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

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

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

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

 

 

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

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

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

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

 

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

 

Post Script

A brief guide to mones

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

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

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

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

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

 

Entomological classics – The Moericke (Yellow) Pan Trap

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

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

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

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

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

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

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

 

References

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

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

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

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

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

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

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

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

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

 

Post script

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