Tag Archives: Drepanosiphum platanoidis

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.

antsaphids-1

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.

antsaphids-2

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.

antsaphids3

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

antsaphids4

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

antsaphids5

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 😦

antsaphids-holdrich

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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Mellow Yellow – Not all aphids live on green leaves

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

leaf roll Rhopalosiphum

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

Leaf roll Myzus cerasi

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

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

Seasonal changes

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

Tar spot 2

Effects of tar spot on sycamore leaves

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

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

Elatobium in action

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

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

References

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

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

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

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

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

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

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

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

Kundu, R. & Dixon, A.F.G. (1994) Feeding on their primary host by return migrants of the host alternating aphid, Cavariella aegopodii. Ecological Entomology, 19, 83-86.

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

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

 

Post script

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

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

 

Post post script

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

Sampsa

 

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

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

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

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

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

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

 

 

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Not all aphids have wings

Given that aphids are commonly known as green-fly or black-fly, it might be presumed that all aphids are capable of flight. Although this is almost certainly universal at the species level (but see Post script) it is not true within a species. As I have described in an earlier post aphids are possessed of extremely complex and fascinating (to me at least) life cycles. Depending on the species, either most stages of the life cycle are winged (alate) as adults, e.g. the sycamore aphid Drepanoisphum platanoidis

Holocyclic.png

Sycamore aphid

I couldn’t resist showing you this beautiful picture of an adult sycamore aphid borrowed from the best aphid web site that I know of (see http://influentialpoints.com/Gallery/Drepanosiphum_platanoidis_common_sycamore_aphids.htm)

 

Other aphid species, such as my favourite, the bird cherry-oat aphid, Rhopalosiphum padi, only produce alate morphs at specific times of year or in response to changes in host plant quality or crowding.

Heteroecious

 RhopalosiphumPadi  Rhopalosiphum padi on leaf

Winged (alate) and non-winged (apterous) morphs of Rhopalosiphum padi.

In species such as the sycamore aphid, the only apterous morph tends to be the sexual female or ovipara, which has no need to disperse and after mating lives only long enough to develop and lay its eggs on the bark of sycamore trees.

Sycamore ovip on bark

Ovipara of the sycamore aphid searching for an oviposition site

In those species such as the bird cherry-oat aphid, the winged forms are very different from the non-winged forms, not just in terms of their wings but in their physiology, behaviour and life history traits (Dixon, 1998). The role of the winged morphs is to find new host plants and to start new colonies. They have long antenna, long legs and well-developed and many, sensory organs (rhinaria). They are the dispersal stage, or in the case of winged males, the mate seekers. They respond more readily to host odours; they need to be able to find new host plants at a suitable physiological stage and preferably free of natural enemies. A well-developed olfactory system is thus called for.

If you cut them open (preferably anaesthetizing them first), and remove their ovaries, you will find that they have ovarioles with only a few embryos in each chain and that most of the embryos are not mature i.e. without eye spots. In addition, if you cut open a number of individuals from the same clone you will find that they will not all have the same number of ovarioles. For example, the alate exules (winged forms produced on the secondary host plants )of Rhoaplosiphum padi, the number of ovarioles can range from four to ten (Wellings et al, 1980). This variability of ovariole number in the dispersal morphs of aphids that spend much of their life cycle on ephemeral host plants is quite common (Leather et al 1988).  So why do so many aphid species have variable numbers of ovarioles in their alate morphs?

Shaw (1970), showed that there appeared to be three types of black bean aphid (Aphis fabae) alate exules; migrants, those that flew before depositing nymphs, flyers, those that deposited a few nymphs before flying, and non-flyers, those that stayed and reproduced on their host plant. He postulated that this was an adaptation in response to host quality, the worse state the plant was in the more likely the migrant morph would be produced. Many years later Keith Walters and Tony Dixon (Walters & Dixon, 1983) were able to show that there was a very strong relationship between reproductive investment (number of ovarioles) and flight willingness and ability. The more ovarioles an aphid had, the less likely it was to want to take off and fly, and in addition those with more ovarioles could not fly for as long or as far as those with fewer.

Ovarioles and flight

In other words a trade-off between fecundity and migration. As long distance aphid migration is very costly (very few survive, Ward et al, 1998) it makes sense to have members of your clone spreading the load (risk), from short-distance hops (trivial flights), with the chance that the next door plant might be just as bad as the one left behind and within easy reach of natural enemies, but with a higher chance of survival and reproduction, to long distance migratory flights, with the reduced probability of finding a host plant but with the chance that it will be high in nutrition and low in natural enemies.

What clever beasts aphids are 😉

 

References

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

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

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

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

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

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

 

Post script

It is possible that there are some aphids that never fly – Aphids from the genus Stomaphis have incredibly long mouthparts (they all feed through tree bark), and as far as I can tell from perusal of

Stomaphis query aceris

Roger Blackman and Vic Eastop’s monumental work, alate morphs have never been described (or seen) and even males are apterous.

Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World’s Trees. CABI, Wallingford.

 

Post post script

For a very detailed and thoughtful review of the ‘decisions’ and costs involved in aphid reproductive and dispersal biology see Ward, S.A. & Dixon, A.F.G. (1984) Spreading the risk, and the evolution of mixed strategies: seasonal variation in aphid reproductive strategies. Advances in Invertebrate Reproduction, 3, 367-386.

 

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Not all aphids aggregate in clumps

There is a tendency for people when they do think of aphids, to see them as existing in large unsightly aggregations, oozing sticky honeydew, surrounded by their shed skins and living in positively slum-like conditions. The bird cherry-oat aphid, Rhopalosiphum padi, the black bean aphid, Aphis fabae, the Poa-feeding aphid, Utamphorophora humboldti and the beech wooly aphid, Phyllaphis fagi, being notable examples.

       Damage on bird cherry             Aphids on runner beans 2014           Office aphids compressed           Beech aphid

Whilst this may be true for many pest aphid species, it is far from true for the group as a whole. Yes they may occur in aggregations, but quite often, they look very neat and tidy and well-behaved.

Conker aphids 2013     Aphids on heath

Some aphid species lead quite solitary lives and you often only find them in ones and twos, if at all, e.g. Monaphis antennata.  There is one aphid species, however, that manages to have it both ways, living surrounded by its friends and relatives but managing to exist in splendid isolation at the same time. The exemplar of this phenomenon is the sycamore aphid, Drepanosiphum platanoidis, which exhibits a behaviour termed ‘spaced-out gregariousness’, a term coined by John Kennedy and colleagues in 1967, although the phenomenon was

sycamore aphids on leaf

described and measured by Tony Dixon a few years earlier. Effectively, the aphids like to be in a crowd but to have their own personal space. As proof of this, when the numbers of aphids on a leaf are low, say two to three, they will, instead of spreading out across the leaf, still show the same behaviour, i.e. get to within 2-3 millimetres distance of each other.

Sycamore compressed

Even more extraordinary is when a predator such as a ladybird or lacewing larvae finds its way on to a crowded leaf; the sycamore aphids do a great imitation of the parting of the Red Sea, but still without touching each other and keeping their regulation distance apart. Those finding themselves at the edge, either take wing or move to the upper surface of the leaf. Although a video of this exists somewhere I have been unable to find it so you will have to take my word for it. If anyone does come across the footage please let me know.

Yet another reason to love aphids.

 

References

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

Kennedy, J.S., Crawley, L., & McLaren, A.D. (1967) Spaced-out gregariousness in sycamore aphids Drepanosiphum platanoides (Schrank) (Hemiptera, Callaphididae). Journal of Animal Ecology, 36, 147-170.

Post script 

You may have noticed that the two references cited spell the species name of the sycamore aphid as platanoides,  It is in fact correctly spelt platanoidis.  To their embarrassment both John Kennedy and Tony Dixon got it wrong.  It wasn’t until 1978, when a very brave (possibly helped by conference alcohol consumption) PhD student (David Mercer) of Tony Dixon’s pointed this out, that the error was noticed and corrected 😉

Reference

Mercer, D.R. (1979) Flight Behaviour of the Sycamore Aphid, Drepanosiphum platanoidis Schr.   Ph.D Thesis, University of East Anglia, Norwich, UK.

 

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A Winter’s Tale – aphid overwintering

Aphids that live in temperate or boreal regions have to be able to survive overwinter. Aphids, depending on species, are able to pass winter in two ways. If they are holocyclic i.e. possess an egg-laying stage, they usually overwinter as eggs. Aphid eggs are extremely cold-hardy; they have been reported to have super-cooling points of about -42oC (Somme ). If laid on a woody host, eggs are usually laid in the bud axils as in the case of the apple aphid, Aphis pomi, the black bean aphid Aphis fabae and the bird cherry aphid, Rhopaloishum padi.

aphid eggs

In some instances, such as the sycamore aphid, Drepanosiphum platanoidis, eggs are laid directly on the tree bark or in crevices in the bark or even in lichen growing on the bark.  See if you can spot the eggs in the picture below.

ovipsyc

If however, the aphid in question lives on an herbaceous host, the eggs may be laid directly on the ground, on or amongst fallen leaves or at the base of grass tussock.

The other strategy adopted by those aphids that are anholocyclic, such as the green spruce aphid, Elatobium abietinum, is to pass the winter as an active stage, either as an adult or immature nymph. Those holocyclic aphids that have anholcyclic strains are also able to adopt this strategy. Despite their soft bodies and fragile appearance, aphids have quite low super-cooling points values such as -26oC having been reported (Griffiths & Wratten, 1979).

A potential advantage of using an active overwintering stage and not an egg, is that if they survive the winter, they are able to start reproducing sooner, particularly if they are a host –alternating aphid, where the aphids hatching from eggs, have to spend time developing and reproducing on the primary woody host before being able to migrate to the secondary hosts. This also applies, to a lesser extent, to those holoyclic aphids living on herbaceous plants, although the temporal advantage is not as great. One would assume that given the relative cold-hardiness attributes of aphid eggs and adults that in a country such as the UK where winter temperatures below -10oC are both infrequent and short lasting, winter survival of aphids would be extremely high if not guaranteed. This is not the case. For example, eggs mortality of the bird cherry aphids is typically around 70-80% as shown in my first ever publication (no fancy graphics packages in those days, just Letraset , Indian ink, stencils and tracing paper). Actually people had measured aphid egg mortality much earlier than this (Gillette, 1908) but I was the first person to monitor mortality throughout the winter and show that it occurred at a steady rate irrespective of the severity of the winter.

 Egg survival

It is actually a function of the length of the winter that determines how many eggs survive, the longer the winter the greater the mortality.

Egg mortality

This level of mortality is typical for all aphid species for which I have data (Leather, 1993). Some of this mortality can be attributed to predation, but most of it is intrinsic (Leather, 1981), possibly due to cryo-injury.

Similarly, those aphids that overwinter as adults or nymphs, despite their ability to super-cool to temperatures below -20oC, experience even greater levels of mortality as shown elegantly by Jon Knight and Jeff Bale in 1986 studying overwinter survival of the grain aphid Sitobion avenae near Leeds.

Knight & Bale

In fact one wonders how any aphids at all survive winter this way, but they certainly do if the winters are mild enough, as in the case of Myzus persicae and Sitobion avenae in southern England and E. abietinum throughout most of its range (Day et al., 2010). An interesting anomaly is Iceland where hot springs abound and the bird cherry aphid is able to survive anholocyclically on grasses growing around the springs whereas in other countries with similar winter temperatures it would only be able to survive as the egg stage.

Despite the importance of winter to aphid population dynamics we still know very little about their winter ecology, our knowledge being confined to a handful of economically important species. Despite the discomfort of field work in the winter this is an area which would be very rewarding to anyone in need of an interesting and good research project.  Finger-less mittens are, however, definitely recommended 😉

Useful references

Bale, J. S. (1996). Insect cold hardiness: a matter of life and death. European Journal of Entomology 93, 369-382. http://www.eje.cz/pdfs/eje/1996/03/09.pdf

Day, K. R., Ayres, M. P., Harrington, R. & Kidd, N. A. C. (2010). Interannual dynamics of aerial and arboreal spruce aphid populations. Population Ecology 52, 317-327. http://link.springer.com/article/10.1007/s10144-009-0190-0#page-1

Gillette, C. P. & Taylor, E. P. (1908). A few orchard plant lice. Colorado Agricultural Experimental Station Bulletin, 113, 1-47.

Griffths, E. &Wratten, S. D. (1979). Intra-and inter-specific differences in cereal aphid low temperature tolerance. Entomologia experimentalis et applicata 26, 161-167. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1979.tb02912.x/abstract

Knight, J. D. & Bale, J. S. (1986). Cold hardiness and overwintering of the grain aphid Sitobion avenae. Ecological Entomology 11, 189-197.

Leather, S. R. (1980). Egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata 27, 96-97. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1980.tb02951.x/abstract

Leather, S. R. (1981). Factors affecting egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Ent omologia experimentalis et applicata 30, 197-199. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1981.tb03097.x/abstract

Leather, S. R. (1993). Overwintering in six arable aphid pests: a review with particular relevance to pest management. Journal of Applied Entomology 116, 217-233. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1993.tb01192.x/abstract;jsessionid=9FC2ED8174E96317F192CF42A19092FE.f03t03?deniedAccessCustomisedMessage=&userIsAuthenticated=false

Strathdee, A. T., Howling, G. G. & Bale, J. S. (1995). Cold hardiness of overwintering aphid eggs. Journal of Insect Physiology 41, 653-657. http://www.sciencedirect.com/science/article/pii/002219109500029T

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Aphid life cycles – bizaare, complex or what?

In a very early post I mentioned that one of the reasons that I love aphids so much is their life-cycles https://simonleather.wordpress.com/aphidology/  and the fantastic jargon that is used to describe them.  Many undergraduates find the jargon off-putting but it was this complexity that really grabbed my imagination.

aphid jargon

Insects are probably the most diverse group of organisms on Earth (Grimaldi & Engel, 2005) and their life cycles range from simple sexual and asexual styles to complex life cycles encompassing obligate and facultative alternation of sexual and asexual components.  Nancy Moran (1992) suggests that in the insect world probably the most intricate and varied life cycles are found in aphids and I certainly wouldn’t disagree.

There are basically two types of aphid life-cycles, non-host alternating (autoecious, monoecious) and host alternating (heteroecious).   Autoecious aphids spend their entire life cycle in association with one plant species as shown below (Dixon, 1985).

autoecious lifecycle

(or group of related plant species), whereas heteroecious aphids divide their time between two very different species of host plant, usually a tree species (the primary host) on which they overwinter, and an herbaceous plant species (the secondary host) on which they spend their summer.

Heteroecious

Approximately 10% of aphid species are heteroecious.  The ancestral aphid life cycle is thought to have been winged, egg laying and autoecious on a woody host plant almost certainly conifers and the oldest families of woody angiosperms e.g. Salicaceae (Mordwilko, 1928; Moran, 1992).

aphid life cycle evolution

Aphid life cycles can also be described as holocyclic, in which cyclical parthenogenesis occurs, with aphids reproducing sexually in the autumn to produce an overwintering egg, in temperate regions and parthenogenetically during spring and summer as shown below for the sycamore aphid (Dixon, 1985).

Holocyclic.png

Some aphids are anholocyclic where the clone is entirely asexual reproducing by parthenogenesis throughout the year. This is often seen in locations where winter conditions are mild, in the tropics for example or as a bit of an oddity around hot-springs in Iceland.

Anholocyclic.png

Parthenogenesis in aphids is coupled with live births and reduced generation times through the phenomenon of telescoping generations.  Parthenogenesis in aphids developed early on but whether the oldest aphids (200 mya) were parthenogenetic is not known.

Host alternation appears to have arisen more than once (Moran, 1988) and occurs in four slightly different forms depending on the taxon in which it occurs.  The main differences being in whether the sexual forms are produced on the primary (winter) host (the host on which the eggs are laid), or as in the case of the Aphidini, the males being produced on the secondary (summer) host and the sexual females produced on the primary host.   The majority of aphids host alternate between unrelated woody and perennial hosts, but some species host alternate between herbaceous plants e.g. pea aphid Acyrthosiphon pisum alternates between the perennial vetches and the annual peas Pisum sativum (Muller & Steiner, 1985) and Urleucon gravicorne alternates between the perennial Solidago and the annual Erigeron (Moran 1983).  Some aphid species such as Rhopalosipum padi, have clones that are holocyclic and some that are anholocyclic, so hedge their bets and also gives me the opportunity to slip in a great slide kindly lent to me by my friend Richard Harrington at Rothamsted Research.

Mixed

One of the things that is rather puzzling is why some aphid species should have adopted a host alternating life cycle which on the face of it, seems to be rather a risky strategy.  You could liken it to looking for a needle in a hay-stack; only about 1 in 300 aphids that leave the secondary host at the end of summer are likely to find their primary host (Ward et al, 1998).  There are a number of theories as to why it has evolved.

1. The nutritional optimization through complementary host growth hypothesis states that heteroecy has been favoured by natural selection because it enables a high rate of nutrient intake throughout the season (Davidson, 1927; Dixon, 1971).  In essence, the clone moves from a host plant where food quality is low and moves onto a herbaceous host that is growing rapidly and thus provides a good source of nutrition.  In autumn, the clone moves back to its primary woody host where leaves are beginning to senesce and provide a better source of nutrition as seen below (Dixon, 1985).

Nutritional changes

On the other hand, non-host alternating aphids such as the sycamore aphid, Drepanosiphum platanoidis, or the maple aphid, Periphyllus testudinaceus, reduce their metabolism and tough it out over the summer months when the leaves of their tree hosts are nutritionally poor, the former as adults, the latter as nymphs (aphid immature forms) known as dimorphs. Mortality over the summer in these species is, however, very high.  In some years I have recorded almost 100% mortality on some of my study trees, so very similar to the 99.4% mortality seen in the autumn migrants (gynoparae) of the bird cherry-oat aphid, Rhoaplosiphum padi.  Other autoecious aphids are able to track resources if they live on host plants that continue to develop growing points throughout the summer.

 Tough it out

Verdict:  No apparent advantage gained

2. The oviposition site advantage hypothesis states that primary woody hosts provide better egg laying sites and provide emerging spring aphids with guaranteed food source (Moran, 1983).  There is however, no evidence that eggs laid on woody hosts survive the winter better than those laid in the herbaceous layer.  Egg mortality in both situations ranges from 70-90% (Leather, 1983, 1992, 1993).

Verdict:  No apparent advantage gained

3.  The enemy escape hypothesis states that by leaving the primary host as natural enemy populations begin to build up and moving to a secondary host largely devoid of enemies confers an advantage on those species that exhibit this trait (Way & Banks, 1968).  At the end of summer, when the natural enemies have ‘found’ the clone again, the clone then migrates back to its primary host, which theoretically is now free of natural enemies.  This is an attractive idea as it is well known that natural enemies tend to lag behind the populations of their prey.

Enemy escape

Verdict: Possible advantage gained

4. The Rendez-vous hosts hypothesis suggests that host alternation assists mate location and enables wider mixing of genes than autoecy (Ward, 1991; Ward et al. 1998).  This seems reasonable, but as far as I know, no-one has as yet demonstrated that host-alternating aphid species have a more diverse set of genotypes than non-host alternating aphids.

Verdict:  Not proven

5.  The temperature tolerance constraints hypothesis which postulates that seasonal morphs are adapted to lower or higher temperatures and that they are unable to exist on the respective host plants at the ‘wrong time of year’ (Dixon, 1985).  I don’t actually buy this one at all, as I have reared spring and autumn morphs at atypical temperatures and they have done perfectly well (Leather & Dixon, 1981), the constraint being the phenological stage of their host plant rather than the temperature.  In addition, there are some host alternating aphid species in which the fundatrix can exist on both the secondary and primary hosts (if the eggs are placed on the secondary host).  This has been experimentally demonstrated in the following species:

Aphis fabae                                 Spindle & bean                                        Dixon & Dharma (1980)

Cavariella aegopdii

Cavariella pastinacea              Willows and Umbelliferae                     Kundu & Dixon (1995)

Cavariella theobaldi

Metopolophium dirhodum       Rose and grasses                                    Thornback (1993)

Myzus persicae                           Prunus spp &  40 different plants       Blackman & Devonshire (1978)

Verdict: Unlikely

6.  The escape from induced host-plant defences hypothesis (Williams & Whitham, 1986), which states that by leaving the primary host as summer approaches, the aphids escape the plant defences being mustered against them.  This is only really applicable to those gall aphids where galled leaves are dropped prematurely by the host plant.

Verdict: Special case pleading?

7.  The constraint of fundatrix specialisation hypothesis is that of Moran (1988), who argues that heteroecy is not an optimal life cycle but that it exists because the fundatrix generation (the first generation that hatches from the egg in spring) on the ancestral winter host, are constrained by their host affinities and are unable to shift to newly available nutritionally superior hosts.  Whilst it is true that some host alternating aphids are however, very host specific as fundatrcies, some aphids are equally host-specific as oviparae at the end of the year the constraints of ovipara specialisation

For example, in the bird cherry-oat aphid Rhopalosiophum padi, the fundatrices are unable to feed on senescent leaf tissue of the primary host, their offspring can only develop very slowly on ungalled tissue and all their offspring are winged emigrants (the alate morph that flies from the primary host to the secondary host) (Leather & Dixon, 1981).  The emigrants are able to feed as nymphs on the primary host on which they develop and as adults on their secondary host, but not vice versa (Leather et al., 1983).  The autumn remigrants (gynoparae, the winged parthenogenetic females that fly from the secondary hosts to the primary hosts on the other hand, feed on the secondary host as nymphs but are unable to feed on the primary host as adults (Leather, 1982; Walters et al., 1984).  The black bean aphid shows similar, but less rigid host specificity and whilst there is a distinct preference for the relevant host plant (Hardie et al., 1989), parthenogenetic forms can occur throughout the summer on the primary host (Way & Banks, 1968), particularly if new growth is stimulated by pruning (Dixon & Dharma, 1980). There are also at least two examples of where both the primary and secondary host are herbaceous (see earlier).  In both these cases the fundatrices could exist on both the primary and secondary host plants

Verdict:  Not proven

So what do I think?  For years I was very firmly convinced that the nutritional optimization hypothesis was the obvious answer; after all Tony Dixon was my PhD supervisor 😉  Now, however, having lectured on the subject to several cohorts of students, if I was forced to pick a favourite from the list above, I would do a bit of fence-sitting and suggest a combination of the nutritional optimization and enemy escape hypotheses. What do you think? There are cetainly a number of possible research projects that would be interesting to follow up, the problem is finding the funding 😦

Sources

Blackman, R.L. & Devonshire, A.L. (1978)  Further studies on the genetics of the carboxylase-esterase regulatory system involved in resistance to orgaophosphorous insecticides in Myzus persicae (Sulzer).  Pesticide Science 9, 517-521

Davidson, J. (1927) The biological and ecological aspects of migration in aphids.  Scientific Progress, 21, 641-658

Dixon, A.F.G. (1971) The life cycle and host preferences of the bird cherry-oat aphid, Rhopalosiphum padi (L) and its bearing on the theory of host alternation in aphids. Annals of  Applied Biology, 68, 135-147.  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1971.tb06450.x/abstract

Dixon, A.F.G. (1985) Aphid Ecology Blackie, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1980.tb02981.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Grimaldi. D. & Engel, M.S. (2005)  Evolution of the Insects, Cambridge University Press, New York

Hardie, J. (1981) Juvenile hormone and photoperiodically controlled polymorphism in Aphis fabae: postnatal effects on presumptive gynoparae. Journal of Insect Physiology, 27, 347-352.

Hardie, J. Poppy, G.M. & David, C.T. (1989) Visual responses of flying aphids and their chemical modification. Physiological Entomology, 14, 41-51.  http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3032.1989.tb00935.x/abstract

Kundu, R. & Dixon, A.F.G. (1995) Evolution of complex life cycles in aphids. Journal of Animal Ecology, 64, 245-255.  http://www.jstor.org/discover/10.2307/5759?uid=3738032&uid=2&uid=4&sid=21102533364873

Leather, S.R. (1982) Do gynoparae and males need to feed ? An attempt to allocate resources in the bird cherry-oat oat aphid Rhopalosiphum padi. Entomologia experimentalis et applicata, 31, 386-390.  http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1982.tb03165.x/abstract

Leather, S.R. (1983) Forecasting aphid outbreaks using winter egg counts: an assessment of its feasibility and an example of its application. Zeitschrift fur  Angewandte  Entomolgie, 96, 282-287. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1983.tb03670.x/abstract

Leather, S.R. (1992) Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis, 17, 101-113.  http://www.cabdirect.org/abstracts/19941101996.html;jsessionid=60EA025C7230C413B6094BCC4966EC06

Leather, S.R. (1993) Overwintering in six arable aphid pests: a review with particular relevance to pest management. Journal of Applied Entomology, 116, 217-233. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0418.1993.tb01192.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on it’s primary host. Annals of applied Biology, 99, 115-118. http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1981.tb05136.x/abstract

Moran, N.A. (1983) Seasonal shifts in host usage in Uroleucon gravicorne (Homoptera:Aphididae) and implications for the evolution of host alternation in aphids. Ecological Entomology, 8, 371-382. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2311.1983.tb00517.x/full

Moran, N.A. (1988) The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. American Naturalist, 132, 681-706. http://www.jstor.org/discover/10.2307/2461929?uid=3738032&uid=2&uid=4&sid=21102533364873

Moran, N.A. (1992) The evolution of aphid life cycles. Annual Review of Entomology, 37, 321-348. http://www.annualreviews.org/doi/abs/10.1146/annurev.en.37.010192.001541

Mordwilko, A. (1928)  The evolution of cycles and the origin of heteroecy (migrations) in plant-lice.  Annals and Magazine of Natural History Series 10, 2, 570-582

Muller, F.P. & Steiner, H. (1985)  Das Problem Acyrthosiphom pisum (Homoptera: Aphididae).  Zietsschrift fur angewandte Entomolgie 72, 317-334

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