Tag Archives: aphids

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 19th Century you can find illustrations such as the one below that appeared in Van Bruyssel’s fantastic foray into early science-communication.

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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.

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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.

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

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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

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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 LasiusEntomologist’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 😦

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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)

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Insects in flight – whatever happened to the splatometer?

I have been musing about extinctions and shifting baselines for a while now; BREXIT and an article by Simon Barnes in the Sunday Times magazine (3rd September 2016) finally prompted me to actually put fingers to keyboard.  I fear that BREXIT will result in even more environmental damage than our successive governments have caused already.  They have done a pretty good job of ignoring environmental issues and scientific advice (badgers) even when ‘hindered’ by what they have considered restrictive European legislation and now that we head into BREXIT with a government not renowned for its care for the environment I become increasing fearful for the environment. Remember who it was who restructured English Nature into the now fairly toothless Natural England, because they didn’t like the advice they were being given and whose government was it who, rather than keep beaches up to Blue Flag standard decided to reclassify long-established resort beaches as not officially designated swimming beaches?  And, just to add this list of atrocities against the environment, we now see our precious ‘green belt’ being attacked.

My generation is liable to wax lyrical about the clouds of butterflies that surrounded us as we played very non PC cowboys and Indians outside with our friends in the glorious sunshine.  We can also fondly reminisce about the hordes of moths that used to commit suicide in the lamp fittings or beat fruitlessly against the sitting room windows at night.  The emptying of the lamp bowl was a weekly ceremony in our house.  We also remember, less fondly, having to earn our pocket-money by cleaning our father’s cars, laboriously scraping the smeared bodies of small flies from windscreens, headlamps and radiator grilles on a Saturday morning.  A few years later as students, those of us lucky enough to own a car, remember the hard to wash away red smears left by the eyes of countless Bibionid (St Mark’s) flies, as they crashed into our windscreens.

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Typical Bibionid – note the red eyes; designed specially to make a mess on your windscreen 🙂 https://picasaweb.google.com/lh/photo/GBgoGHhRbj-eUUF9SxZ4s9MTjNZETYmyPJy0liipFm0?feat=embedwebsite

Are these memories real or are we looking back at the past through those rose-tinted glasses that only show the sunny days when we lounged on grassy banks listening to In the Summertime and blank out the days we were confined to the sitting room table playing board games?

We have reliable and robust long-term data sets showing the declines of butterflies and moths over the last half-century or so (Thomas, 2005; Fox, 2013) and stories about this worrying trend attract a lot of media attention. On a less scientific note, I certainly do not find myself sweeping up piles of dead moths from around bedside lamps or extricating them from the many spider webs that decorate our house.  Other charismatic groups, such as the dragonflies and damselflies are also in decline (Clausnitzer et al., 2009) as are the ubiquitous, and equally charismatic ground beetles (carabids) (Brooks et al., 2012).  But what about other insects, are they too on the way out?  A remarkable 42-year data set looking at the invertebrates found in cereal fields in southern England (Ewald et al., 2015) found that of the 26 invertebrate taxa studied less than half showed a decrease in abundance; e.g. spiders, Braconid parasitic wasps, carabid beetles, Tachyporus beetles, Enicmus (scavenger beetles), Cryptophagid fungus beetles, leaf mining flies (Agromyzids), Drosophila, Lonchopteridae (pointed wing flies), and surprisingly, or perhaps not, aphids.  The others showed no consistent patterns although bugs, excluding aphids, increased over the study period.  Cereal fields are of course not a natural habitat and are intensely managed, with various pesticides being applied, so are perhaps not likely to be the most biodiverse or representative habitats to be found in the UK.

But what about the car-smearing insects, the flies, aphids and other flying insects?  Have they declined as dramatically?  My first thought was that I certainly don’t ‘collect’ as many insects on my car as I used to, but is there any concrete evidence to support the idea of a decline in their abundance.  After all, there has been a big change in the shape of cars since the 1970s.

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Top row – cars from 1970, including the classic Morris 1000 Traveller that my Dad owned and I had to wash on Saturdays.

Bottom row the cars of today, sleek rounded and all looking the same.

 

Cars were  much more angular then, than they are now, so perhaps the aerodynamics of today’s cars filter the insects away from the windscreen to safety? But how do you test that?  Then I remembered that the RSPB had once run a survey to address this very point.  Sure enough I found it on the internet, the Big Bug Count 2004, organised by the RSPB.  I was very surprised to find that it happened more than a decade ago, I hadn’t thought it was that long ago, but that is what age does to you 🙂

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The “Splatometer” as designed by the RSPB

The idea, which was quite cool, was to get standardised counts of insect impacts on car number platesThe results were thought to be very low as the quote below shows, but on what evidence was this based?

“Using a cardboard counting-grid dubbed the “splatometer”, they recorded 324,814 “splats”, an average of only one squashed insect every five miles. In the summers of 30-odd years ago, car bonnets and windscreens would quickly become encrusted with tiny bodies.”  “Many people were astonished by how few insects they splatted,” the survey’s co-ordinator Richard Bashford, said.

Unfortunately despite the wide reporting in the press at the time, the RSPB did not repeat the exercise.  A great shame, as their Big Garden Birdwatch is very successful and gathers useful data.   So what scientific evidence do we have for a decline in these less charismatic insects?  Almost a hundred years ago, Bibionid flies were regarded as a major pest (Morris, 1921) and forty years ago it was possible to catch almost 70 000 adults in a four week period from one field in southern England (Darcy-Burt & Blackshaw, 1987).   Both these observations suggest that in the past Bibionids were very common.  It is still possible to pluck adult Bibionids out of the air (they are very slow, clumsy fliers) in Spring, but if asked I would definitely say that they are not as common as they were when I was a student.  But as Deming once said, “Without data, you’re just another person with an opinion.”  In the UK we are fortunate that a long-term source of insect data exists, courtesy of Rothamsted Research, the longest running agricultural research station in the world.  Data have been collected from a nationwide network of suction and light traps for more than 50 years (Storkey et al., 2016).   Most of the publications arising from the survey have tended to focus on aphids (Bell et al., 2015) and moths (Conrad et al., 2004), although the traps, do of course, catch many other types of insect (Knowler et al., 2016).  Fortuitously, since I was interested in the Bibionids I came across a paper that dealt with them, and other insects likely to make an impact on cars and splatometers (Shortall et al., 2009).  The only downside of their paper was that they only looked at data from four of the Rothamsted Suction Traps, all from the southern part of the UK, which was a little disappointing.

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Location and results of the suction traps analysed by Shortall et al. (2009).

Only three of the trap showed downward trends in insect biomass over the 30 years (1973-2002) analysed of which only the Hereford trap showed a significant decline.  So we are really none the wiser; the two studies that focus on a wider range of insect groups (Shortall et al., 2009; Ewald et al., 2015) do not give us a clear indication of insect decline.   On the other hand, both studies are limited in their geographic coverage; we do not know how representative the results are of the whole country.

What a shame the RSPB stopped collecting ‘splatometer’ data, we would now have a half-decent time series on which to back-up or contradict our memories of those buzzing summers of the past.

Post script

After posting this I came across this paper based on Canadian research which shows that many pollinators, possibly billions are killed by vehicles every year.

References

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

Brooks, D.R., Bater, J.E., Clark, S.J., Montoth, D.J., Andrews, C., Corbett, S.J., Beaumont, D.A., & Chapman, J.W. (2012) Large carabid beetle declines in a United Kingdom monitoring network increases evidence for a widespread loss of insect biodiversity. Journal of Applied Ecology, 49, 1009-1019.

Clausnitzer, V., Kalkman, V.J., Ram, M., Collen, B., Baillie, J.E.M., Bedjanic, M., Darwall, W.R.T., Dijkstra, K.D.B., Dow, R., Hawking, J., Karube, H., Malikova, E., Paulson, D., Schutte, K., Suhling, F., Villaneuva, R.J., von Ellenrieder, N. & Wilson, K. (2009)  Odonata enter the biodiversity crisis debate: the first global assessment of an insect group.  Biological Conservation, 142, 1864-1869.

Conrad, K.F., Woiwod, I.P., Parsons, M., Fox, R. & Warren, M.S. (2004) Long-term population trends in widespread British moths.  Journal of Insect Conservation, 8, 119-136.

Darcy-Burt, S. & Blackshaw, R.P. (1987) Effects of trap design on catches of grassland Bibionidae (Diptera: Nematocera).  Bulletin of Entomological Research, 77, 309-315.

Ewald, J., Wheatley, C.J., Aebsicher, N.J., Moreby, S.J., Duffield, S.J., Crick, H.Q.P., & Morecroft, M.B. (2015) Influences of extreme weather, climate and pesticide use on invertebrates in cereal fields over 42 years. Global Change Biology, 21, 3931-3950.

Fox, R. (2013) The decline of moths in Great Britain: a review of possible causes. Insect Conservation & Diversity, 6, 5-19.

Knowler, J.T., Flint, P.W.H., & Flint, S. (2016) Trichoptera (Caddisflies) caught by the Rothamsted Light Trap at Rowardennan, Loch Lomondside throughout 2009. The Glasgow Naturalist, 26, 35-42.

Morris, H.M. (1921)  The larval and pupal stages of the Bibionidae.  Bulletin of Entomological Research, 12, 221-232.

Shortall, C.R., Moore, A., Smith, E., Hall, M.J. Woiwod, I.P. & Harrington, R. (2009)  Long-term changes in the abundance of flying insects.  Insect Conservation & Diversity, 2, 251-260.

Storkey, J., MacDonald, A.J., Bell, J.R., Clark, I.M., Gregory, A.S., Hawkins, N. J., Hirsch, P.R., Todman, L.C. & Whitmore, A.P. (2016)  Chapter One – the unique contribution of Rothamsted to ecological research at large temporal scales Advances in Ecological Research, 55, 3-42.

Thomas, J.A. (2005) Monitoring change in the abundance and distribution of insects using butterflies and other indicator groups.  Philosophical Transactions of the Royal Society B, 360, 339-357

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Ideas I had and never followed up

“When I was younger, so much younger than before” I never needed any help to come up with ideas for research topics or papers.   When I was doing my PhD and later as a post-doc, I used to keep a note pad next to my bed so that when I woke up in the middle of night with an idea (which I often did) I could scribble it down and go back to sleep.  (These days sadly, it is my bladder and not ideas that wake me up in the wee small hours 🙂*)

On waking up properly, these ideas, if they still seemed sensible, would  move onto Stage 2, the literature search.  In those days, this was much more difficult than it is now, no Google Scholar or Web of Science then, instead you had to wade though the many hard-copy Abstract series and then get hard copies of the papers of interest.  Once in my hands, either via Inter-library loans or direct from the author, or even photocopied from the journal issue (we did have photocopiers in those days), the papers would be shoved into a handy see-through plastic folder (Stage 3).  Depending on how enthusiastic I was about the idea, I would then either mock-up a paper title page or put the folder in the ‘to deal with later’ pile (Stage 4).   Many of these eventually led on to Stage 5, experiments and published papers.  Others have languished in their folders for twenty or thirty years.

As part of my phased run up to retirement (2021), I have started farming out my long-term publishable (hopefully) data-sets to younger, more statistically astute colleagues and ‘publishing’ less robust, but possibly useful data on my blog site.  I have also, somewhat halfheartedly since the task is monumental, started to go through my old field and lab books that

monumental-data

A monumental collection of data.  The top right picture is my 20-year sycamore data set.  I estimate that there are about 7 million data points in it; of which to date only 1.6 million, give or take a million, are computerised.  I also have a ten-year bird cherry aphid data set from Scotland, waiting to go on the computer, any volunteers?

are not yet computerised.  Whilst doing this I came across some Stage 3 folders, which as you can see from the colour of the paper have languished for some time.

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The Forgotten Nine

 

There were nine forgotten/dismissed proto-papers, the oldest of which, judging by the browning of the paper and my corresponding address, dates from the early 1980s, and is simply titled “What are the costs of reproduction?”.  This appears to have been inspired by a talk given by Graham Bell at a British Ecological Society, Mathematical Ecology Group meeting in 1983.  In case you are wondering, this was one of those meetings supposed to bring theorists and empiricists together.   It didn’t work, neither group felt able to talk to each other 🙂  The idea, inevitably based on aphid data, didn’t bear any fruit, although I do have this graph as a souvenir.  If anyone wants

graph

In those days we used graph paper 🙂

 the data, do let me know.

Slightly later, we find the grandly titled, “Size and phylogeny – factors affecting covariation in the life history traits of aphids”.  This had apparently been worked up from an earlier version of a paper, less grandly, but no less ponderously, titled, “Size and weight: factors affecting the level of reproductive investment in aphids”.  This is based on some basic dissection data from eight aphid species and presents the relationships, or lack of, between adult weight (or surrogate measure), ovariole number, potential fecundity and the number of pigmented embryos.  As far as I can remember these are data that Paul Wellings** and I collected as a follow-up to work we had published from a side project when we were doing our PhDs at the University of East Anglia (Wellings et al., 1980).  The second title was inspired by a paper by Stephen Stearns (Stearns, 1984), who was something of a hero of mine at the time, and was, I guess, an attempt to publish pretty simple data somewhere classier than it deserved 🙂  So this one seems to be a Stage 4, almost Stage 5 idea, and may, if I have time or someone volunteers, actually get published, although I suspect it may only make it to a very minor journal under its original title.

Then we have a real oddity, “Aphids, elephants and oaks: life history strategies re-examined”.  This one as far as I remember, is based on an idea that I had about r- and k-selection being looked at from a human point of view and not the organism’s point of view.  My thesis was that an oak tree was actually r-selected as over its life-time it was more fecund than an aphid 🙂  I suspect this was going to be aimed at the Forum section of Oikos.

The next one, dates from the late-1980s, “Protandry versus protogyny: patterns of occurrence within the Lepidoptera”, and reflects the fact that females of the pine beauty moth, Panolis flammea, on which I was then working, emerge before the males (Leather & Barbour, 1983; Leather, 1984), something not often reported in Lepidoptera.  I wondered what advantage (if any) this gave P. flammea.  I planned this one as a review or forum type paper but never got beyond the title and collecting two references (Robertson, 1987; Zonneveld & Metz, 1991).  I still think this is an interesting idea, but do feel free to have a go yourselves, as again, I suspect that I won’t actually get round to it.

Finishing off my time in Scotland, is a paper simply entitled, “Egg hatch in the bird cherry aphid, Rhopalosiphum padi.” I have ten years of egg hatch data from eight trees waiting to be analysed.  This is almost certainly not worth more than a short note unless I (or a willing volunteer) tie it in with the ten years data on spring and autumn populations on the same trees 🙂 Aphid egg data although not very abundant, is probably not in great demand.  My first published paper (Leather, 1980) was about egg mortality in the bird cherry aphid and 36 years later has only managed to accrue 32 citations, so I guess not an area where one is likely to become famous 🙂

I then have four papers dating from my time as an Associate Member of the NERC Centre for Population Biology at Silwood Park.   The first is titled, “The suitability of British Prunus species as insect host plants” and was definitely inspired by my foray into counting host plant dots as exemplified by the late great Richard Southwood (Leather, 1985, 1986).  I think I was going to look at palatability measures of some sort.

The next is called ‘Realising their full potential: is it important and how many insects achieve it?”  I’m guessing that this was a sort of follow-up to my second most-cited paper ever (Leather, 1988), the story of which you can read here, if at all interested.  Most insects, even those that are pests, die before achieving anywhere near their full reproductive potential, but then so do we humans, and our population continues to grow.  So in answer to the question, I guess not and no it doesn’t matter 🙂

Also linked to insect reproduction is the next paper, which I have followed up with the help of a PhD student, and do hope to submit in the near future, “Queue positions, do they matter”.  As this one may actually see the light of day, I won’t say anything further about it.

And finally, another one about aphid eggs, “Bud burst and egg hatch synchrony in aphids”.  This one was going to be based on my then ten-year sycamore aphid data but is now based on my twenty-year data set and is now in the very capable hands of a PhD student and hopefully will see the light of day next year.

There are also a number of other folders with no titles that are just full of collections of reprints.  I can only guess at what these ideas were so won’t burden you with them.

I mentioned at the beginning of this piece that I don’t wake up in the middle of the night with ideas any more.  As we get older I think there is a tendency to worry that we might run out of ideas, especially when, as we do in the UK, suffer from ludicrously underfunded research councils with very high rejection rates that don’t allow you to resubmit failed grant applications.  It was thus reassuring to see this recent paper that suggests that all is not lost after you hit the grand old age of 30.  That said, I do believe that as you move away from the bench or field, the opportunity to be struck by what you see, does inevitably reduce.  As a PhD student and post-doc you are busy doing whatever it is you do, in my case as an ecological entomologist, counting things, and inevitably you see other things going on within and around your study system, that spark off other ideas.  It was the fear of losing these opportunities as I moved up the academic ladder, which inevitably means, less field and bench time and more time writing grant applications and sitting on committees, that I specifically set aside Monday mornings (very early mornings) to my bird cherry plots and even earlier Thursday mornings to survey my sycamore trees.   Without those sacrosanct mornings I am pretty certain I would have totally lost sight of what is humanly possible to do as a PhD student or post-doc.  This, thankfully for my research group, means that I had, and have, realistic expectations of what their output should be, thus reducing stress levels all round.   As a side benefit I got to go out in the fresh air at least twice a week and do some exercise and at the same time see the wonderful things that were going on around and about my study areas and as a bonus had the chance to get some new ideas.

 

References

Leather, S.R. (1984) Factors affecting pupal survival and eclosion in the pine beauty moth, Panolis flammea (D&S). Oecologia, 63, 75-79.

Leather, S.R. (1985) Does the bird cherry have its ‘fair share’ of insect pests ? An appraisal of the species-area relationships of the phytophagous insects associated with British Prunus species. Ecological Entomology, 10, 43-56.

Leather, S.R. (1986) Insect species richness of the British Rosaceae: the importance of host range, plant architecture, age of establishment, taxonomic isolation and species-area relationships. Journal of Animal Ecology, 55, 841-860.

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. & Barbour, D.A. (1983) The effect of temperature on the emergence of pine beauty moth, Panolis flammea Schiff. Zeitschrift fur Angewandte Entomologie, 96, 445-448.

Robertson, H.G. (1987) Oviposition and site selection in Cactoblastis cactorum (Lepidoptera): constraints and compromises. Oecologia, 73, 601-608.

Stearns, S.C. (1984) The effects of size and phylogeny on patterns of covariation inthe life history traits of lizards and snakes. American Naturalist, 123, 56-72.

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.

Zonneveld, C. & Metz, J.A.J. (1991) Models on butterfly protandry – virgin females are at risk to die. Theoretical  Population Biology, 40, 308-321.

 

*I hasten to add that I do still have new ideas, they just don’t seem to wake me up any more 🙂

**Now Vice-Chancellor of the University of Wollongong

 

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Filed under Science writing, Uncategorized

Red, green or gold? Autumn colours and aphid host choice

“The falling leaves
Drift by my window
The falling leaves
Of red and gold”

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Red, green and gold, all on one tree

When Frank Sinatra sang Autumn Leaves he was almost certainly not thinking of aphids and I am pretty certain that the English lyricist, Johnny Mercer, who translated the words from the original French by Jacques Prévert wasn’t either 🙂

The colours we see in autumn are mainly due to two classes of pigment, the carotenoids (yellow-orange; think carrot) and the anthocyanins (red-purple).  Carotenoids are present in the leaves all year round but are masked by the green chlorophyll.  Chlorophyll breaks down in autumn, leaving the yellow carotenes visible.  The anthocyanins on the other hand are not formed until autumn (Sanger, 1971; Lee & Gould, 2002) and this mixture of pigments give us the colours that have inspired so many artists.

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Autumn Leaves Georgia O’Keeffe (1924) Tate Modern

To many, autumn starts with the appearance of the first turning leaves, to me it is the arrival of gynoparae* of the bird cherry-oat aphid (Rhopalosiphum padi) on my bird cherry (Prunus padus) trees.

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Bird cherry, Prunus padus, leaves on the turn.

Little did I know when I started my PhD in 1977 that almost thirty years later I would be part of a raging debate about the function of autumn colouration in woody plants. At the time I was interested in the colonisation patterns (or as I pretentiously termed it in my thesis ‘remigration’) of bird cherry aphids from their secondary grass and cereal host plants to their primary host bird cherry.  My study system was 30 bird cherry saplings divided between two cold frames in the Biology Compound at the University of East Anglia (Norwich).  Every day from the middle of August until leaf fall I checked every leaf of each tree, for gynoparae, males and oviparae, carefully noting the position of each leaf, its phenological stage and giving it a unique number. I repeated this in the autumns of 1978 and 1979.  The phenological stage was based on the leaf colour: green, mature; yellow, mature to senescent; red, senescent.  What I reported was that more gynoparae landed on green and yellow leaves than on red and that the gynoparae on green and yellow leaves survived for longer and produced more offspring (oviparae), than those on red leaves (Leather, 1981).   The gynoparae of the bird cherry aphid are quite special in that although as adults they do not feed (Leather, 1982), they do not land on bird cherry trees at random (Leather & Lehti, 1982), but choose trees that not only do their offspring (the oviparae) do better on, but that also favour those aphids hatching from eggs in the spring (Leather, 1986).  It should not have come as a surprise then, that when I analysed some of the data I had collected all those years ago, their preference for green and yellow leaves over red ones, is linked to how long those

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Figure 1. Length of time leaves remained on tree after first colonisation by gynoparae of Rhopalosiphum padi (F = 30.1 df 2/77, P <0.001)

leaves have left to live (Figure 1). The timing of events at this time of year, has, of necessity, got to be very precise. The egg-laying females (oviparae) are unable to develop on mature bird cherry leaves (Leather & Dixon, 1981), but it seems that the bird cherry aphid has this under control, making its decisions about the timing of the production of autumn forms (morphs) sometime in August (Ward et al., 1984).  All very sensible as far as I was concerned and that was as far as I took things.  Subsequent work by Furuta (1986) supported this in that he showed that maple aphids settled on and reproduced on green-yellow and yellow-orange leaves but avoided red leaves which had shorter life spans.

Jump forward fifteen years or so, and in a paper, that at the time, had somehow passed me by, the late great Bill Hamilton and Sam Brown (Hamilton & Brown, 2001) hypothesised that trees with an intense autumn display, similarly to those brightly coloured animals that signal their distastefulness with yellows, blacks and reds, were signalling their unsuitability as a host plant to aphids.  Like the costs imposed on insects that sequester plant toxins to protect themselves against predators, the production of anthocyanins responsible for the red autumn colouration is expensive, especially when you consider that the leaves have only a short time left to live (Hoch et al., 2001).  In autumn, trees and woody shrubs are normally mobilising resources in the leaves and moving them back into themselves ready to be used again the following spring (Dixon, 1963). Ecologists and evolutionary biologists were thus keen to explain the phenomenon in terms of trade-offs, for example, fruit flags that advertise the position of fruits for those trees that rely on seed dispersal by vertebrates (Stiles, 1982) or as ultra-violet screens to prevent tissue damage (Merzlyak & Gittelson, 1995).  Hamilton & Brown felt that these hypotheses were either, in the case of the fruit flag, only applicable to trees with fruit present and, in the latter, untenable. Instead they advocated the ‘signalling hypothesis’ which was based on the premise that trees that suffer from a lot of aphids (attacked by more than one species rather than by large numbers of a single species), invest in greater levels of defence and in autumn advertise this using bright warning colours.   The premise being, that although it is metabolically expensive for the plants to produce these colours, it is worth the investment if they result in a reduction in aphid attack.

This hypothesis was not without its detractors. Others suggested, that far from avoiding red colours, aphids were attracted to yellow or green as an indicator of host nutrition (Wilkinson et al., (2002).  Holopainen & Peltonen (2002) also suggested that birch aphids use the onset of autumn colours to pick out those trees where nutrient retranslocation was happening, and thus with higher levels of soluble nitrogen in the leaves.  This was of course, what I was trying to confirm back when I was doing my PhD.  Conversely, supporters of the signalling hypothesis, argued that trees (birch again) that could ‘afford’ to produce bright autumn colours were fitter, so more resistant in general and that they were warning potential herbivores of this by a bright autumn display (Hagen et al 2004).

Round about this time (2002), I was approached by a young Swiss researcher, Marco Archetti, who knew that I had a plot of sixty bird cherry trees that I had planted up when I arrived at Silwood in 1992, originally designed to follow-up some work that I had begun whilst at the Forestry Commission looking at the effects of early season defoliation on subsequent tree growth (Leather, 1993, 1995).  Marco convinced me that I had the ideal set-up to test the ‘signalling hypothesis’ and what was to be a very fruitful collaboration began.

We counted arriving gynoparae and their offspring (oviparae) throughout October (Marco making trips over from Oxford where he was then based**) noting leaf colour before and after each count.  As with my PhD work we found that the greener trees were preferentially colonised by the gynoparae and that more oviparae were produced on those trees and that given what I had found earlier that bird cherry aphid gynoparae chose trees that are good hosts in spring (Leather, 1986), Marco felt that we were able to support the honest signalling hypothesis (Archetti & Leather, 2005).  I was slightly less comfortable about this, as there are only two species of aphid that attack bird cherry and one of those is very rare and the original signalling hypothesis was based on the premise that it was trees that were attacked by a lot of aphid species that used the red colouration as a keep clear signal.  Anyway, it was published 🙂

That said, others agreed with us, for example, Schaefer & Rolshausen (2006) who called it the defence indication hypothesis, arguing that bright colours advertise high levels of plant defence and that the herbivores would do well to stay away from those plants displaying them. On the other hand, Sinkkonen (2006) suggested that reproductively active plants produce autumn colours early to deter insects from feeding on them and thus reduce their seed set.

Chittka & Döring (2007) on the other hand, suggested that there is no need to look further than yellow carotenoids acting as integral components of photosynthesis and protection against light damage and red anthocyanins preventing photo-inhibition (Hoch et al., 2001) as to why trees turn colourful in autumn.  In other words, nothing to do with the insects at all.  A couple of years later however, Thomas Döring and Marco got together with another former colleague of mine from Silwood Park, Jim Hardie, and changed their minds slightly.  This time, whilst conceding that red leaves are not attractive to aphids but noting that yellow leaves are even more attractive than green ones, suggested that the red colour could be being used to mask yellow (Döring et al., 2009).

Others have their own pet theories.  In recent years, veteran Australian entomologist Tom White has become interested in the concept of insect species that specifically feed on senescent plant tissue (White, 2002, 2015) and added to the debate by suggesting that aphids in general are senescence feeders and thus choose green and yellow as they have longest time to live and that the red leaves are also nitrogen depleted (White, 2009) which is supported by my PhD data (Figure 1).  This resulted in a spirited response by Lev-Yadun & Holopainen (2011) who claimed that he had misunderstood the scenario in thinking that leaves go sequentially from green to yellow to red, which they suggest is rare (I question this) and that actually in trees that go from green to red, the leaves still contain significant amounts of nitrogen, so a deterrent signal is still required.

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Maple, green to yellow in this case

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Spindle, Euonymus europaeus, green to red

What about those trees and other plants that have red or purple leaves in the spring or all year round and not just in autumn?

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Some trees have red foliage all year

Trees like some of the ornamental cherries or copper beech? I haven’t been able to find any papers that suggest that red or purple-leaved varieties of beech and cherries are less susceptible to aphid attack.  My own observations, probably imperfectly recalled, are that copper beech is regularly infested by the beech woolly aphid, Phyllaphis fagi , and just as heavily, if not more so than the normal green-leaved  beech trees.  That of course may just be a reflection that the white waxy wool covering the aphid stands out more against the red leaves.  Perhaps someone out here might like to check this out?  Some work that my friend and former colleague, Allan Watt, (sadly unpublished) did many years ago in Scotland looking at the effect of beech species and cultivar on infestation levels by the beech leaf mining weevil, Rhynchaenus fagi, did not indicate any differences between copper and green cultivars.  It does seem however, that in cabbages, leaf colour can tell the specialist cabbage aphid, Brevicoryne brassciae, if plants are well defended or not, the bluer the cabbage, the nastier it is (Green et al, 2015).

To summarise:

  1. Red leaves are produced by the trees in autumn to reduce ultraviolet damage and protect metabolic processes in the leaf.
  2. Red leaves are deliberately produced by the tree to warn aphids that their leaves are well defended – honest signalling.
  3. Red leaves are produced by the tree to ‘fool’ the herbivores that the leaves are likely to drop soon and warn them to keep away so as to safeguard their fruit – dishonest signalling.
  4. The tree is blissfully unaware of the aphids and the aphids are exploiting the intensity of the autumn colours produced by the trees to select which are the best trees to colonise in terms of nutrition and length of time left on the tree.

As I write, the debate still goes on and we seem no nearer to arriving at a definitive answer to the riddle of why trees produce bright leaves in autumn.  If nothing else however, the debate has generated a lot of interest and enabled people to sneak some amusing titles into the scientific literature.  Do make the effort to read the titles of some of the references below.

References

Archetti, M. (2009) Phylogenetic analysis reveals a scattered distribution of autumn colours. Annals of Botany, 103, 703-713.

Archetti, M. & Leather, S.R. (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus.  Oikos, 110, 339-343.

Chittka, L. & Döring, T.F. (2007) Are autumn foliage colors red signals to aphids? PLoS Biology , 5(8): e187. Doi:10.1371/journal.pbio.0050187.

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

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

Furuta, K. (1986) Host preferences and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera: Aphididae). Zeitschrift fur Angewandte Entomologie, 102, 93-100.

Green, J.P., Foster, R., Wilkins, L., Osorio, D. & Hartley, S.E. (2015) Leaf colour as a signal of chemical defence to insect herbivores in wild cabbage (Brassica oleracea).  PLoS ONE, 10(9): e0136884.doi:10.1371/journal.pone.0136884.

Hagen, S.B. (2004) Autumn coloration as a signal of tree condition. Proceedings of the Royal Society London B, 271, S184-S185.

Hamilton, W.D. & Brown, S.P. (2001) Autumn tree colours as handicap signal. Proceedings of the Royal Society London B, 268, 1489-1493.

Hoch , W.A.,  Zeldin, E.L. & McCown, B.H. (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology, 21, 1-8.

Holopainen, J.K. & Peltonen, P. (2002) Bright colours of deciduous trees attract aphids: nutrient retranslocation hypothesis.  Oikos, 99, 184-188.

Leather, S.R. (1981) Reproduction and survival: a field study of the gynoparae of the bird cherry-oat aphid, Rhopalosiphum padi (L.). Annales Entomologici Fennici, 47, 131-135.

Leather, S.R. (1982) Do gynoparae and males need to feed? An attempt to allocate resources in the bird cherry-oat aphid Rhopalosiphum padiEntomologia experimentalis et applicata, 31, 386-390.

Leather, S.R. (1986) Host monitoring by aphid migrants: do gynoparae maximise offspring fitness? Oecologia, 68, 367-369.

Leather, S.R. (1993) Early season defoliation of bird cherry influences autumn colonization by the bird cherry aphid, Rhopalosiphum padi. Oikos, 66, 43-47.

Leather, S.R. (1995) Medium term effects of early season defoliation on the colonisation of bird cherry (Prunus padus L.). European Journal of Entomology, 92, 623-631.

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on its primary host. Annals of Applied Biology, 99, 115-118.

Leather, S.R. & Lehti, J.P. (1982) Field studies on the factors affecting the population dynamics of the bird cherry-oat aphid, Rhopalosiphum padi (L.) in Finland. Annales Agriculturae Fenniae, 21, 20-31.

Lee, D.W. & Gould, K.S. (2002) Anthocyanins in leaves and other vegetative organs: An introduction. Advances in Botanical Research, 37, 1-16.

Lev-Yadun, S. & Holopainen, J.K. (2011) How red is the red autumn leaf herring and did it lose its red color? Plant Signalling & Behavior, 6, 1879-1880.

Merzlyak, W.N. & Gittelson, A. (1995) Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescing leaves (Acer platanoides L.). Journal of Plant Physiology, 145, 315-320.

Sanger, J.E. (1971) Quantitative investigations of leaf pigments from their Inception in buds through autumn coloration to decomposition in falling leaves.  Ecology, 52, 1075-1089.

Schaefer, H.M. & Rolshausen, G. (2006) Plants on red alert – do insects pay attentionBioEssays, 28, 65-71.

Sinkkonen, A. (2006) Do autumn leaf colours serve as reproductive insurance against sucking herbivores?  Oikos, 113, 557-562.

Stiles, E.W. (1982) Fruit flags: two hypotheses. American Naturalist, 120, 500-509.

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

White, T.C.R. (2003) Nutrient translocation hypothesis: a subsect of the flush-feeding/senescence-feeding hypothesis. Oikos, 103, 217.

White, T.C.R. (2009) Catching a red herring: autumn colours and aphids. Oikos, 118, 1610-1612.

White, T.C.R. (2015) Senescence-feesders: a new trophic subguild of insect herbivore. Journal of Applied Entomology, 139, 11-22.

Wilkinson, D.M., Sherratt, T.N., Phillip, D.M., Wratten, S.D., Dixon, A.F.G. & Young, A.J. (2002) The adaptive significance of autumn colours.  Oikos, 99, 402-407.

 

 *for a detailed account of the wonderful terminology associated with aphid life cycles read here

**coincidentally he is now a Lecturer at the University of East Anglia in the same Department where I did my PhD

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Filed under Aphidology, Aphids, Science writing

An aphid is… a flea, a louse, and even a marine mammal!

Earlier this year I wrote about the debate that rages about the correct way to talk about thrips during which I got distracted and ended up writing about their names in different languages. It turns out that I am not alone in being curious about international insect naming. I have just finished reading Matthew Gandy’s excellent book Moth, where he waxes lyrical about the different names used to describe butterflies and moths around the world.  This, of course, made me wonder what aphid would turn up, so armed with dictionaries and Google Translate, I traveled the world to see what I could discover.

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The bronze-brown dandelion aphid, Uroleucon taraxaci – Photo by Jasper Hubert

There are a lot of languages so I am only going to highlight a few versions of aphid that I found interesting or surprising.  According to The Oxford English Dictionary, Linneaus coined the word Aphides, which may (or not) have been inspired by the Ancient Greek  ἀφειδής‎ (apheidḗs) meaning unsparing, perhaps in relation to their rapid reproduction and feeding habits.  The modern spelling of aphid seems to have come into being after the Second World War, although you could still find aphides being used in the late 1940s (e.g. Broadbent et al., 1948; Kassanis, 1949), and it can still be found in more recent scientific literature where the journal is hosted in a non-English speaking country.

Many aphid names are very obviously based on the modern Latin word coined by Linneaus, although in some countries more than one name can be used, as in the UK where aphid is the technical term but blackfly and green-fly are also commonly used.

 

Aphide derived names

Albanian              afideja

English                  aphid

French                  aphide

Hindu                    एफिड ephid

Portuguese         afídio

Spanish                áfido

 

More common are those names that relate to the vague resemblance that aphids have to lice and to their plant feeding habit. The term plant lice to describe aphids was commonly used in the scientific literature up and into the early 1930s (e.g. Mordvilko, 1928; Marcovitch, 1935).

 

Names linked to the putative resemblance to lice and their plant feeding habit

Bosnian                lisna uš                 uš is louse, lisna derived from leaf

Bulgarian             listna vŭshka     vŭshka louse, listna plant leaf

Danish                  bladlaus               blad is leaf, laus louse

Dutch                    bladluis                blad is leaf, luis is louse

Estonian               lehetäi                  leht is leaf, tai is louse

German                Blattlaus               blatt is leaf, laus is louse

Greek                   pseíra ton fytón louse on plant

Hungarian           levéltetű               leve is leaf, tetű is louse

Icelandic              lús or blaðlús     lús is louse, blað is plant

Latvian                  laputs                   lapa is, uts is louse

Norwegian          bladlus                 blad is plant, lus is louse

Swedish               bladlus                 as for Norwegian

 

If you draw siphunculi on to a louse and add a cauda to the rear end you can just about see the resemblance.

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Louse with added siphunculi and cauda

 

Names based on the premise that aphids resemble fleas

French  puceron                  puce is flea

Spanish pulgón                   pulga is flea

anaphidis-3-jpg

Flea with cauda and siphunclus, but still only a poor imitation of the real thing.  Even with added aphid features I don’t see the resemblance 🙂

 

In Turkish, aphid is yaprak biti which roughly translates to leaf biter.  There are then a few languages where there appears to be no connection with their appearance or feeding habit.

 

Other names for aphid

Basque                 zorri

Chinese                蚜

Filipino                 dapulak

Finnish                  kirva

Lithuanian           Mszyca

Tamil                     அசுவினி Acuviṉi

Welsh                   llyslau

Xhosa                    zomthi

 

In Lithuanian, where aphid is Mszyca, which looks like it might be derived from Myzus, an important aphid genus, aphid also translates to amaras which means blight.  In the case of a heavy aphid infestation, this is probably an apt description.  I was also amused to find that whilst the Welsh have a name for aphid, Scottish Gaelic does not.

My all-time favourite, and one for which I can find no explanation at all, is dolphin.  According to Curtis (1845), aphids on cereals in some counties of England were known as wheat dolphins.  I was also able to trace the use of this name back to the previous century (Marsham, 1798), but again with no explanation why this name should have arisen.

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The wheat dolphin 🙂

References

Broadbent, L., Doncaster, J.P., Hull, R. & Watson, M.A. (1948) Equipment used for trapping and identifying alate aphides.  Proceedings of the Royal Entomological Society of London (A), 23, 57-58.

Curtis, J. (1845) Observations on the natural history and economy of various insects etc., affecting the corn-crops, including the parasitic enemies of the wheat midge, the thrips, wheat louse, wheat bug and also the little worm called Vibrio. Journal of the Royal Agricultural Society, 6, 493-518.

Gandy, M. (2016) Moth, Reaktion Books, London

Kassanis, B. (1949) The transmission of sugar-beet yellows virus by mechanical inoculation. Annals of Applied Biology, 36, 270-272.

Marcovitch, S. (1935) Experimental evidence on the value of strip farming as a method for the natural control of injurious insects with special reference to plant lice. Journal of Economic Entomology, 28, 62-70.

Marsham, T. (1798) XIX. Further observations on the wheat insect, in a letter to the Rev. Samuel Goodenough, L.L.D. F.R.S. Tr.L.S.  Transactions of the Linnaean Society of London, 4, 224-229.

Mordvilko, A. (1928) LXX.—The evolution of cycles and the origin of Heteroecy (migrations) in plant-lice , Annals and Magazine of Natural History: Series 10, 2, 570-582.

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It isn’t easy being an applied ecologist – working on crops limits publication venues

“This is Simon Leather, he’s an ecologist, albeit an applied one” Thus was I introduced to a group of visiting ecologists by my then head of department at the Silwood Park campus of Imperial College. As you can imagine I was somewhat taken aback at this public display of the bias that ‘pure’ scientists have against those that they regard as ‘applied’.  I was (and still am), used to this attitude, as even as an undergraduate doing Agricultural Zoology when we shared modules with the ‘pure’ zoologists, we were regarded as a slightly lower life form J  Working in Finland as a post-doc in the early 1980s it was also obvious that there was a certain degree of friction between the pure and applied entomologists, so it was not a phenomenon confined entirely to the UK.  To this day, convincing ecology undergraduates that integrated pest management is a suitable career for them is almost impossible.

I was an ecologically minded entomologist from early childhood, pinning and collecting did not interest me anywhere near as much as insect behaviour and ecology, but I knew that I wanted to do something “useful” when I grew up. Having seen my father in action as a plant pathologist and crop protection officer, it seemed to me that combining entomology with agriculture would be an ideal way to achieve this ambition.  A degree in Agricultural Zoology at Leeds and a PhD in cereal aphid ecology at the University of East Anglia (Norwich) was the ideal foundation for my chosen career as an applied ecologist/entomologist.

I started my professional life as agricultural entomologist working both in the laboratory and in the field (cereal fields to be exact), which were easily accessible, generally flat, weed free and easy to manipulate and sample.  In the UK even the largest fields tend to be visible from end to end and side to side when you stand in the middle or edge (even more so now than when I started as wheat varieties are now so much shorter, less than half the height they were in 1977).

applied-fig-1

 

Having fun as a PhD student – aphid ‘sampling’ in Norfolk 1978

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I haven’t grown since I did my PhD so wheat must have shrunk 🙂

See the post script to see what wheat used to look like.

Laboratory experiments, even when working on mature plants were totally do-able in walk-in growth rooms, and at a push you could even fit whole earing wheat plants into a growth cabinet.

I then spent ten years working as a forest entomologist, where field sites were the exact opposite, and extreme measures were sometimes required to reach my study animals, including going on an official Forestry Commission tree climbing course.

applied-fig-3

Pole pruners – (of only limited use) and tree climbing (great fun but laborious)

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Scaffold towers for really high work, but expensive (and scary on sloping hillsides).

And as for lab work, not a chance of using mature plants or even plants more than two to three years old.  Excised branches and/or foliage (rightly or wrongly) were the norm*.

Doing field work was, despite the sometimes very physically challenging aspects, a lot of fun, and in my case, some very scenic locations.  My two main field sites were The Spey Valley and

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Sutherland and Caithness, both of which provided magnificent views and of course, a plethora of whisky distilleries

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where I discovered what is now my favourite single malt 🙂

The real fun came when it was time to submit papers.  Journal choice was (and is) very important.  As Stephen Heard points out, journals have a ‘culture’ and it is very important to pick a journal that has the right editorial board and ethos. The laboratory work never seemed to be a huge problem, referees (perhaps wrongly) very rarely criticised the use of young plants or excised foliage. I was able to publish the output from what was a very applied project, in a range of journals from the very specialised to the more ecological. This selection for example, from 1985-1987 (Leather, 1985, 1986; Leather & Burnand, 1987; Leather et al., 1985), appeared in Ecological Entomology, Oecologia, Functional Ecology and Bulletin of Entomological Research respectively.

Papers reporting field-based work were a little bit harder to place in journals outside the mainstream forestry ones, particularly when it came to experimental work.  One of the problems was that ecological referees unused to working in forests tended not to have a grasp of what was involved in setting up and servicing an experiment in a forest plantation or stand.  A farmer has no great objection to an entomologist removing 100 wheat tillers a week from his 2 ha field (at 90 stems per metre2, even a 16 week field season would only remove a tiny fraction of his crop).  A forest manager on the other hand with a stocking density of 3000 stems per hectare would look askance at a proposal to remove even 100 trees a month from a hectare plot, especially if this was repeated for seven years.  Sample size was thus a problem, even when using partial sampling of trees, e.g. by removing say only one branch.  When it came to field scale replication, to compare for example, three treatments and a control on two different soil types, where each treatment plot is a hectare, things get a bit difficult. The most that we could service, even with help (since we did not have huge financial resources), was three replicates of each treatment.  In agricultural terms this seems incredibly low, where 10m2 plots or even smaller, are very often used (e.g. Staley et al., 2009; Garratt et al., 2011).

We thus ended up with our experimental papers in the really specialised forestry journals (e.g.  Leather, 1993; Hicks et al., 2007).  On the other hand, those papers based on observational, long-term data were easier to place in more general ecological journals (e.g. Watt et al., 1989), although that was not always enough to guarantee success (e.g. Walsh et al., 1993; Watt et al., 1991).  Another bias that I came across (perhaps unconscious) was that referees appeared, and still do, think that work from production forests is not as valid as that coming from ‘natural’ forests, especially if they are tropical. We came across this when submitting a paper about the effects of prescribed burning on carabid populations in two sites in Portugal (Nunes et al., 2006).  We originally sent this to a well-known ecological journal who rejected it on the grounds of low replication, although we had also replicated it temporarily as well as geographically.  I was not impressed to see a paper published in this journal shortly after they had rejected our manuscript in which the authors had reported changes in insect communities after a one-off fire event in a tropical forest, without even the benefits of pre-fire baseline data.  We had in the meantime, given up on general ecology journals and submitted our paper to a local forestry journal.  Such is life.

I originally started this essay with the idea of bemoaning the fact that publishing studies based in production forests in more general journals was more difficult than publishing agriculturally based papers, but got diverted into writing about the way applied ecologists feel discriminated against by journals and pure ecologists.  I may or may not have convinced you about that.  To return to my original idea of it being more difficult for forestry–based ecologists to break out of the forestry journal ghetto than it is for agro-ecologists to reach a broader audience, I present the following data based on my own publication record, which very convincingly demonstrates that my original feeling is based on fact, albeit based on an n of one 🙂

applied-fig-7

Numbers of agricultural and forestry based papers published by me in different journal categories.

I might also add that being an entomologist also limits where you can publish, so being an applied entomologist is something of a double whammy, and when it comes to getting research council funding, don’t get me started!

References

 Garratt, M.P.D., Wright, D.J., & Leather, S.R. (2010) The effects of organic and conventional fertilizers on cereal aphids and their natural enemies. Agricultural and Forest Entomology, 12, 307-318.

Hicks, B.J., Aegerter, J.N., Leather, S.R., & Watt, A.D. (2007) Differential rates of parasitism of the pine beauty moth (Panolis flammea) depends on host tree species. Scottish Forestry, 61, 5-10.

Leather, S.R. (1985) Oviposition preferences in relation to larval growth rates and survival in the pine beauty moth, Panolis flammea. Ecological Entomology, 10, 213-217.

Leather, S.R. (1986) The effect of neonatal starvation on the growth, development and survival of larvae of the pine beauty moth Panolis flammea. Oecologia, 71, 90-93.

Leather, S.R. (1993) Influence of site factor modification on the population development of the pine beauty moth (Panolis flammea) in a Scottish lodgepole pine (Pinus contorta) plantation. Forest Ecology & Management, 59, 207-223.

Leather, S.R. & Burnand, A.C. (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D&S): the hidden costs of reproduction. Functional Ecology, 1, 331-338.

Leather, S.R., Watt , A.D., & Barbour, D.A. (1985) The effect of host plant and delayed mating on the fecundity and lifespanof the pine beauty moth,  Panolis flammea (Denis & Schiffermuller) (Lepidoptera: Noctuidae): their influence on population dynamics and relevance to pest management. Bulletin of entomological Research, 75, 641-651.

Nunes, L.F., Silva, I., Pité, M., Rego, F.C., Leather, S.R., & Serrano, A. (2006) Carabid (Coleoptera) community change following prescribed burning and the potential use of carabids as indicator species to evaluate the effects of fire management in Mediterranean regions. Silva Lusitania, 14, 85-100.

Staley, J.T., Stewart-Jones, A., Pope, T.W., Wright, D.J., Leather, S.R., Hadley, P., Rossiter, J.T., Van Emden, H.F., & Poppy, G.M. (2010) Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments. Proceedings of the Royal Society of London B, 277, 779-786.

Walsh, P.J., Day, K.R., Leather, S.R., & Smith, A.J. (1993) The influence of soil type and pine species on the carabid community of a plantation forest with a history of pine beauty moth infestation. Forestry, 66, 135-146.

Watt, A.D., Leather, S.R., & Stoakley, J.T. (1989) Site susceptibility, population development and dispersal of the pine beauty moth in a lodgepole pine forest in northern Scotland. Journal of Applied Ecology, 26, 147-157.

Watt, A.D., Leather, S.R., & Evans, H.F. (1991) Outbreaks of the pine beauty moth on pine in Scotland: the influence of host plant species and site factors. Forest Ecology and Management, 39, 211-221.

 

Post script

The height of mature wheat and other cereals has decreased hugely over the last two hundred years.  Cereals were originally a multi-purpose crop, not just providing grain for humans, but bedding straw for stock and humans, winter fodder for animals, straw for thatching and if really desperate, you could make winter fuel out of discarded straw**.

applied-fig-8

John Linnell  – Wheat 1860  You wouldn’t have been able to see Poldark’s (Aidan Turner) manly chest whilst he was scything in this field!

aplied-fig-8

Pieter Breugel the Elder – Die Kornernter – The Harvesters  (1565) – Head-high wheat crops and not just because the average height was lower in those days.

 

*As I was writing this article I came across this paper (Friberg & Wiklund, 2016) which suggests that using excised plants may be justifiable.  Friberg, M. & Wiklund, C. (2016)  Butterflies and plants: preference/performance studies in relation to plant size and the use of intact plants vs. cuttings.  Entomologia experimentalis et applicata, 160, 201-208

**My source for this is Laura Ingalls Wilder – Little House on the Prairie, to be exact 🙂

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Getting a buzz with science communication – Reflections on curating Realscientists for a week

My week on Realscientists was a direct result of National Insect Week, a biennial event organised by the Royal Entomological Society (RES) to bring the wonders of entomology to a wider audience*. I had never thought about being a curator for Realscientists although I have followed them for some time.  Back in February however, one of my PhD students who has been involved with National Insect Week on more than one occasion, suggested that I might apply to curate RealScientists during National Insect Week as the RES Director of Outreach, Luke Tilley, was hoping to be on Biotweeps during National Insect Week as well.  To make sure that I had no excuse to forget to do it, she very helpfully sent me the link to the Realscientists web site and instructions on how to apply 🙂

Duly briefed, I contacted Realscientists and to my surprise and slight apprehension, was given the slot I had asked for, the week beginning 19th June.  As my curatorial stint drew closer I began to worry about what I was going to tweet about and how to fit it into my day-to-day activities.

I made a list of twenty pre-planned Tweets to give me an outline script to work from. I managed to include all but one into my week as curator, the one about why you should want to work in entomology.

RS1

The twenty tweet list

I felt that my whole week was addressing this point so there was no need to belabour the point any more.  I also received an email from Realscientists with a Vade Mecum of how and what to tweet.  I was somewhat concerned by the section on how to deal with trolling, but I needn’t have worried, as far as I could tell I received no overt abuse**.

The big day approached, which as my actual launch was at Sunday lunchtime caused some slight logistical problems, but easily solved by making lunch a bit later than usual. As it was a Sunday I basically kept it light, introduced myself and tweeted a few insect factoids and pictures, including some great images from van Bruyssels The Population of an Old Pear Tree.  I have my own hard copy of the 1868 translated edition, but if you want to read it on-line it is available here.

RS2a

From van Bruyssel – The Population of an Old Pear Tree

It is definitely worth a read.

I also had to make a decision about how much time I was going to spend Tweeting. The previous curator had only done about 10-15 tweets a day, which is what I usually do.  The curator before her, however, had done considerably more.  As my stint as curator coincided with National Insect Week and as my contract with my university does actually specify that I do outreach***, I felt that I could justify several hours a day to it and that is what I did, and managing to fit quite a bit of the day job in between.

In between tweeting images and fantastic insect facts I tried to get some important messages across to my audience.  I started with what some might  term a “conservation rant”, basically bemoaning the fact that although insects make up the majority of the animal kingdom, conservation research and funding is very much biased toward the vertebrates, largely those with fur and feathers.  I also pointed out that most statements about how we should go about conservation in general is based on this unbalanced and not very representative research.  Taxonomic chauvinism has annoyed my for a long time 🙂

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That rant over I introduced my audience to the work our research group does, biological control, chemical ecology, integrated pest management, agro-ecology and urban ecology and conservation. Our use of fluorescent dust and radio tagging to understand insect behaviour aroused a lot of interest and comment.

 RS4

Using alternative technology to understand vine weevil behaviour.

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The glow in the dark sycamore aphid was also very popular

 

Midweek I translated one of my outreach talks to Twitter and in a frenzy of Tweets introduced the world to Bracknell and the biodiversity to be found on its roundabouts and how an idea of how to teach locally relevant island biogeography and conservation, turned into a 12 year research project.

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How teaching led research – the Bracknell roundabout story.

In between these two main endeavours, I tweeted about the influences that entomology has had on art, literature, popular culture, religion, medicine, engineering, advertising, economics, medicine , fashion and even advertising, using a variety of images.

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Our new insect-inspired smoke detector attracted a lot of love and envy.

I even composed a haiku for the occasion

Six-legged creatures;

Fascinating and diverse,

Beautiful insects

 

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I have been an entomologist for a long time.

and told the story of my life-long love of insects, incidentally revealing some of my past hair-styles and exposing my lack of interest in sartorial elegance 🙂

My overall message for the week was, and hopefully I got this across, is that we should be much

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more aware of what is under our feet and surrounding us and of course, that aphids are not just fantastic insects

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My final tweet

but also beautiful animals.

Giant Myzus

Model Myzus persicae that I recently met in the Natural History Museum

And finally, would I do it again? Yes most definitely. I ‘met’ a lot of new and very interesting people and had some really good ‘conversations’.

 

References

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

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

Leather, S. R. (2009). Taxonomic chauvinism threatens the future of entomology. Biologist 56, 10-13.

 

 

*I was one of the original ‘founders’ of National Insect Week so have always tried to be involved in some way with the event.

**or I am so thick-skinned I didn’t notice it 🙂

***or as Harper Adams University quaintly terms it, “reach out”

 

 

 

 

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

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

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

View

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

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

Grant

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

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

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

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

Graph

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

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

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

References

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

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

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

Leather, S.R. (1989) Phytodecta pallida (L.) (Col.,Chrysomelidae) – a new insect record for bird cherry (Prunus padus). Entomologist’s Monthly Magazine, 125, 17-18.

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

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

 

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

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

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

 

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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).

Symbionts

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

Pea aphids colour

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.

Glossary

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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

Lost 1

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).

Lost 2

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.

Lost 3

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).

Lost 4

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

Lost 5

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

Lost 6

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.

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