Sometimes big can be good – Reflections on INTECOL 2013

Warning:  I am not going to discuss the science presented, just my impressions of the conference as a whole.

In April I wrote about my dislike of big international conferences  citing reasons such as  the difficulty in finding people, session clashes, people giving talks on already published papers and the tendency of just talking to people you already know.  I finished the article somewhat cynically, with the phrase “perhaps INTECOL will prove me wrong”; for those of you who may not know, INTECOL is the acronym of the International Association for Ecology (I had to look it up myself to get it exactly right).  INTECOL 2013 (#INT13 for Twitter users) coincided with the 100^th birthday of the British Ecological Society and was held at the ExCel Centre in London.  It thus promised to be a very large event.  So two strikes against it already as far as I was concerned, huge conference and in London, probably my least favourite city of all time; twenty years of commuting into the South Kensington campus of Imperial College from Bracknell has not left me pleasant memories and although having had a cosmopolitan childhood I am a small village boy at heart.  I probably wouldn’t have gone to INTECOL at all, if the British Ecological Society hadn’t subsidised my attendance (I am an Associate Editor for the Journal of Animal Ecology) and we hadn’t taken our summer holiday earlier than usual this year.  I decided that I would commute in daily, rather than pay for accommodation; we still have a house in Bracknell, despite me working in Shropshire, and it would also give me the opportunity to have some family time.

For me the conference started on Sunday morning when my wife and I travelled into the ExCel Centre to set up the Harper Adams University display stand.  This was done very quickly and we then went for a walk in the sunshine to look at the surrounding area with the impressive London Dockers statue just outside the ExCel , and the street food outlets down near the

Emirates Air Lines (cable cars across the  Thames) and an abortive trip to look at the London Olympic site (no access available); luckily next to the Westfield Shopping Centre, so some entertainment there;  people watching from the M&S Café on the Bridge and a free taster glass of the new Pimms flavour, blackberry and elderflower.  Then back to the ExCel for the very pleasant welcome mixer, where as I had predicted I spoke to people I already knew and then back home to Bracknell.  I was up very early on Monday to catch the dreaded Reading to Waterloo slow service (65 minutes from Bracknell to Waterloo) and then the 40 minute tube and DLR journey from Waterloo to Prince Regent and the ExCel.  Things were very busy but as I had volunteered to do student talk judging, my schedule was fixed for me for the first two days; no need to wade through the huge programme and sigh over clashes.   At the first plenary it was announced that questions would only be taken via Twitter; there were a few disgruntled groans from the audience but as a Twitter convert of less than a year, I was intrigued and  it also gave me an idea.  There and then I decided that I would try to say hello in person to as many people I could find who followed me on Twitter, my fellow Tweeps.  I had a mission and I have to admit it made the meeting quite fun, instead of waiting for people to say hello and mainly just talking to old friends I was on the hunt; as an entomologist it reminded me very much of my childhood days of insect collecting.  This was also made easier by the very user-friendly delegate badges, actually readable at a distance and here I at least, was very pleased with the draconian attitude of the ExCel

security staff who insisted that badges were worn at all times by delegates.  It always annoys me when delegates don’t wear their badges and when the lettering is so small that you have to get embarrassingly close to people’s vital areas to identify them 😉  Note that in the picture above the lanyard is positioned to prevent the badge turning round and being unreadable; many people used the central hole which meant that their badges were often totally useless as a means of identification.

At first I took a few of my ex-students to task (of which there were many) and showed them how to wear their badges.  I may then have become somewhat evangelical, indeed officious, about the subject and started teaching strangers how to wear their badges correctly;

no matter I had a mission and was enjoying the conference and meeting lots of new people. The second conference-changing moment was the plenary lectures and asking questions via Twitter, or Tweeqs as I called them.  One problem I did have, was that I found it difficult to type and listen at the same time; how do students manage in lectures?  I also found that although you could ask a question there was then no chance to riposte when the speaker answered verbally to the whole audience, so no real debate, but I think it has potential.  For example, my question to Georgina Mace, who gave a very good lecture on biodiversity conservation in the 21^st Century but largely ignored invertebrates when making assumptions and predictions about the future, was not entirely answered to my

satisfaction, being along the lines of yes I know that data are not balanced but we are waiting for you guys to produce similar data sets, did generate some Twitter debate but I was not able to respond directly to Georgina.  Still, I think that this is definitely an

creative way forward and allows people not at a conferences to ‘attend’.  I especially highlight this for the benefit of Chris Buddle of McGill University and Blogger extra-ordinaire at Arthropod Ecology, who although not at INTECOL, was able to participate, albeit only at a distance (from Canada to be precise).

Perhaps at future meetings there may be some way to employ an official conference tweeter (or more), akin to the way translators are used at the United Nations?

I also very much enjoyed meeting many of the next generation of ecologists as well as chatting to many ex-students and colleagues.  I would especially like to highlight the fact that Kathryn Luckett, a PhD student at Silwood Park, publicised, first via Twitter and secondly by her recent blog post, about the inequality in ecology of career progression for female scientists as very well illustrated by the presenters at the conference.

 

I think that this is something for us all to think very hard about. and I urge you to read her post.

Commuting as I was, meant that I was not as able to take part in the social events to the same extent as those staying in the very nearby hotels, healthier for both my wallet and my liver, although that said I did pick up a cold – not sure who to blame for that, the daily tube journey or the influx of delegates from all around the world!

The programme overall was excellent, the speakers in the main, fantastic, and the organisation by the BES and local committee very good indeed.  I would have liked it better if the coffee and tea had been on tap all day and not at set times.  The BES Centenary party was a superb idea, even though I had to leave before the band started!  So on the whole; I actually enjoyed this conference very much but I am not sure how much I gained scientifically.  I do think, however, that everyone had a great time and I certainly made many useful contacts, although as predicted there were a number of people who I wanted to see who I never did manage to find.  Well done BES and INTECOL for putting on such a great event. It is always good to be proved wrong once in a while, especially if it is a pleasant surprise.

The week after next, I am presenting a talk at ENTO13 at St Andrews University, on the usefulness of social media for scientists.  This will be a much smaller conference, albeit international.  I wonder if I will enjoy it as much or more?

Post script – for those of you curious about the stand, here is a picture of it with me and Fran Sconce (a PhD student of mine working on Collembola) in attendance.  Note that we are both wearing butterfly themed clothing – how entomological can you get 😉 and our badges are the right way round.

Saproxylicphilia – dead wood alive and well

As some of my followers on Twitter will know, I have the habit of when certain so-called general ecology and conservation journals issue their new contents list, of highlighting how few invertebrate papers have been published in that particular issue.  The journal Animal Conservation, has often been the recipient of my Tweets in that they, despite their name, pretty much ignore most of the animal world, concentrating instead on those minority organisms, the vertebrates and then, mainly mammals.

I was thus a little surprised when at the beginning of June I received an email from the Editorial Office of Animal Conservation asking me if I would be willing to provide a commentary piece on a paper that would be coming out shortly

From: Elina Rantanen

Sent: 05 June 2013 14:11

To: Simon Leather

Subject: Animal Conservation – Invitation to write a commentary for Feature Paper

 Dear Prof. Leather,

 I am writing on behalf of the Editors of Animal Conservation to enquire whether you would be interested in writing a short commentary on a paper which will be published in our August issue.  The paper (attached) is entitled: ‘Protected areas and insect conservation: questioning the effectiveness of Natura 2000 network for saproxylic beetles in Italy’ by Manuela D’Amen et al. We would be delighted if you would be willing to contribute.

 By way of background, the editors of Animal Conservation select a topical article in each issue, and invite experts in the field to provide short commentaries on the study.  These commentaries are then published alongside the original paper, together with a concluding piece by the original authors.  The intention of the commentaries is to discuss the findings of the study and to draw out some of their wider implications.

 Commentaries can also be used to critique a study and can generate debate although this is not the primary intention.  We normally aim to publish about three commentaries with every highlighted article.  The commentaries are usually about 1,000 words in length, and do not require an abstract.  If you agree, I would need to receive your commentary by 19th June. The commentary will be checked by the Editor of the Feature paper before it is accepted.

 If you would like to see examples of previous commentaries, please visit the Animal Conservation homepage: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-1795 where previous featured articles and commentaries are available with free access.

 Please let me know as soon as possible whether or not you will be able to accept this invitation.

 I look forward to hearing from you – it would be great to have you involved.

 Kind regards,

 Elina

 Dr. Elina Rantanen

Editorial Office, Animal Conservation

I was of course hoist with my own petard and had no other choice but to agree.  Actually, I was delighted and grateful to have the opportunity.

The paper, by D’Amen and colleagues dealt with the mismatch between the Natura 2000 network and the conservation of saproxylic beetles in Italy.  The authors pointed out that basically saproxylic beetles were badly served by the network in Italy which had been designed with the large charismatic mega-fauna in mind, and not the small things that run the World.  This of course allowed me a platform from which to further highlight yet another example of institutional vertebratism and reiterate my call for a less biased approach to conservation and ecology in general, which I was very happy to do indeed.

It was while I was writing this that I came across a blog post by Jeff Ollerton of Northampton University in which whilst discussing the huge amount of pollination literature that today’s PhD students are faced with, he described a phenomena that he aptly called The Cliff

Now it just so happens that I have recently had a PhD student successfully defend her thesis on saproxylic beetles and their natural enemies.  Her PhD was a follow-up to another one of my former students who investigated the volatiles given off by those fungi that cause the decay in dead and dying trees.  In addition, in my role of Editor-in-Chief of Insect Conservation & Diversity, I have noticed an increasing number of papers on saproxylic insects being submitted to the journal.  Jeff’s article thus stimulated me to see if there was also a cliff effect in the saproxylic literature.  I thus turned to that invaluable source of data, the Web of Knowledge and using the terms saproxylic , and saproxylic  beetles set the search going.   I did indeed find a Cliff effect, albeit slightly later than the pollination one.  The first published item appeared to be in 1976 which is surprising as according to Grove (2002), the term was first coined by Dajoz in France in 1966.  I have, however, so far been unable to find this paper to confirm this assertion.  Apparently, prior to Dajoz, anything that fed on wood, dead or alive, was termed xylophagous or as a xylobiont.  It was perhaps Martin Speight’s ground breaking report of 1989 extolling the importance of the dead wood habitat that caused the first cliff in about 1991.  This was followed by another ten years later or so, and since then there has been a huge increase in interest in the subject.  The incomplete data for 2013 indicate that the trend is still upwards.  Most work appears to be on beetles which given their relative abundance, makes sense.

  

So, yes here we have another example of a step change in a research area.  I wonder how many more examples there are out there and if it is possible to tie them in to a particular government policy or influential publication.

References

Dajoz R. (1966) Ecologie et biologie des coléoptères xylophages de la hêetraie. Vie Milieu 17:525–636

Grove,  S. J. (2002). Saproxylic insect ecology and the sustainable management of forests. Annual Review of Ecology and Systematics 33: 1-23.  http://www.annualreviews.org/doi/abs/10.1146/annurev.ecolsys.33.010802.150507?journalCode=ecolsys.1

Speight MCD. 1989. Saproxylic Invertebrates and their Conservation. Strasbourg, Fr: Counc. Eur. 79 pp.

In case you wondered

What is Natura 2000 ?

Natura 2000 is the centrepiece of EU nature & biodiversity policy. It is an EUwide network of nature protection areas established under the 1992 Habitats Directive. The aim of the network is to assure the long-term survival of Europe’s most valuable and threatened species and habitats. It is comprised of Special Areas of Conservation (SAC) designated by Member States under the Habitats Directive, and also incorporates Special Protection Areas (SPAs) which they designate under the 1979 Birds Directive. Natura 2000 is not a system of strict nature reserves where all human activities are excluded. Whereas the network will certainly include nature reserves most of the land is likely to continue to be privately owned and the emphasis will be on ensuring that future management is sustainable, both ecologically and economically.  The establishment of this network of protected areas also fulfills a Community obligation under the UN Convention on Biological Diversity.

http://ec.europa.eu/environment/nature/natura2000/

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.

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).

(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.

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 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).

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.

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.

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).

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.

 

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.

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

Thornback, N. (1983)  The Factors Determiining the Abundance of Metopolophium dirhodum (Walk.) the Rose Grain Aphid.  PhD Thesis, University of East Anglia.

Walters, K.F.A., Dixon, A.F.G., & Eagles, G. (1984) Non-feeding by adult gynoparae of Rhopalosiphum padi and its bearing on the limiting resource in the production of sexual females in host alternating aphids. Entomologia experimentalis et applicata, 36, 9-12. http://onlinelibrary.wiley.com/doi/10.1111/j.1570-7458.1984.tb03398.x/abstract?deniedAccessCustomisedMessage=&userIsAuthenticated=true

Ward, S.A. (1991). Reproduction and host selection by aphids: the importance of ‘rendevous’ hosts. In Reproductive Behaviour of Insects: Individuals and Populations (eds W.J. Bailey & J. Ridsdill-Smith), pp 202-226. Chapman & Hall, London.

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. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2656.1998.00238.x/full

Way, M.J. & Banks, C.J. (1968) Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter host Euonymus europaeus L. Annals of Applied Biology, 62, 177-197.  http://onlinelibrary.wiley.com/doi/10.1111/j.1744-7348.1968.tb02815.x/abstract

Williams, A.G. & Whitham, T.G. (1986) Premature leaf abscission: an induced plant defense against gall aphids. Ecology, 67, 1619-1627.  http://www.jstor.org/discover/10.2307/1939093?uid=3738032&uid=2&uid=4&sid=21102533364873