Not all aphids are farmed by ants

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Aren’t insects wonderful?

 

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

*in my opinion at any rate 🙂

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

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

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

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

 

Post script

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

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

Ten papers that shook my world – watching empty islands fill up – Simberloff & Wilson (1969)

Sadly this is the tenth and last in my series of the ten papers that had a great influence on my life as an ecologist.  I’m going to cheat somewhat and actually discuss three papers. In my defence they are extremely closely linked and I am pretty certain that in today’s publishing world they would all have had to have been combined anyway.  That aside, I really liked this experiment the first time I read about it and still rate it very highly.  I would, however, love to be able to travel back in time and give them a couple of hints with the benefit of hind-sight, although as the authors are two of the greatest living ecologists, Dan Simberloff and E O Wilson, I might be a bit apprehensive doing so 🙂 In any case, much of what I would have said was addressed a few years later (Simberloff, 1976).

Wilson and Simberloff wanted to practically test the island biogeography theory famously described by McArthur and Wilson a few year earlier (MacArthur & Wilson, 1967).  To do this they travelled to the Florida Keys and after due reconnaissance decided that the many mangrove “tree islands” would be ideal study sites (Figure 1).  Then came the really cool bit.

Figure 1.  Two of the experimental ‘islands’ from Wilson & Simberloff (1969)

They set about removing the arthropod animal life from nine of the islands (Figure 2), or as much as they could, by fogging with methyl bromide; not something we could do now.  They then monitored the islands at frequent intervals for the next year.  They had of course surveyed the islands before they fumigated them.

Figure 2.  What a cool project; defaunation in progress – from Wilson & Simberloff (1969)

Figure 3. Island equilibria – from Simberloff & Wilson (1970)

The major finding from their study was that recolonization happened quite quickly and that a year later had pretty much reached an equilibrium position (Figure 3).  Another important finding and one that has important implications for restoration and conservation strategies was that two years after the defaunation event, although the islands were well populated, the species composition, except for one island was less than 40% similar to the original inhabitants (Simberloff & Wilson (1970).  Most species present were new to those islands.  The analysis of the data presented in the two data papers is rather basic, some of the key island biogeographical premises are not addressed at all and I wondered why they had not done so.  Their data are all shown in some detail so it is possible to do some more analysis, which I took the liberty of doing.  The extra analysis shows why they did not discuss area effects per se .  The only significant relationship that I could find was that between the number of species and the distance from the ‘mainland’ source (Figure 4), which as predicted by MacArthur & Wilson (1967) was negative. Sadly, island size did not correlate with species number (Figure5).   Finally, there was a positive, but not significant relationship between the initial number of species found on an island and the number a year later (Figure 6).

Figure 4.  Relationship between distance from ‘mainland’ source and the number of arthropod species present (R² = 0.65, P <.0.05) Data from Simberloff & Wilson (1970).

Figure 5.  Island diameter and number of arthropod species (not statistically significant, r² = 0.19, although I am sure many politicians would view this as a positive trend). Data from Simberloff & Wilson (1970)

Figure 6.  Initial number of species on an island and number of species present one year later. Although it looks convincing (r² = 0.54), there are too few observations to reach statistical significance.  Data from Simberloff & Wilson (1970)

Although this work was extremely influential, (my Bracknell roundabouts study owes a lot to it), there were two major flaws in the original experimental design.  Firstly the number of islands was very low, but of course this is understandable, given the effort and complex logistics required to remove the arthropods safely (Figure 2).  The other flaw was that the islands did not cover a large enough range of sizes, thus making it less likely for the species-area pattern to be detected which was a great shame.

As I mentioned earlier, these short-comings were not ignored by the authors, and a few years later Sinberloff (1976) reported the results of an enhanced study, again in the Florida Keys, where he was able to convincingly demonstrate the species-area effect.   I guess that this was pretty satisfying as it tied up a number of loose strings.  He also managed to get the phrase “flogging a dead horse” into his introduction 🙂

Of the three papers, Simberloff & Wilson (1969) is the most highly cited (according to Google Scholar, 618 to date) and became a “citation classic”* in 1984 at which time it had accumulated 164 citations.  Simberloff & Wilson (1970) has attracted 252 cites with Wilson & Simberloff (1969) trailing in third with a mere 158 cites.  As a point of interest, Simberloff (1976) has so far received 313 cites.  To reiterate, the original mangrove island study, despite its flaws was a fantastic piece of work and Sinberloff and Wilson won the Mercer Award of the Ecological Society of America for this work in 1971.

I can think of no better person to explain why Simberloff & Wilson (1969) deserves its place in the Ecological Hall of Fame than Simberloff himself who in the commentary to the 1984 citation classic article wrote “I think the main reason it is cited, however, and its lasting contribution, is not so much that it supports the [equilibrium] theory, as that it reported a field experiment on ecological communities, and thus seemed dramatically different from the correlative approach that dominated this field”

 

References

MacArthur, R.H. & Wilson, E.O. (1967) The Theory of Island Biogeography Princeton University Press, Princeton.

Simberloff, D. (1976)  Experimental zoogeography of islands: effects of island size.  Ecology, 57, 629-648.

Simberloff, D. & Wilson, E.O. (1969) Experimental zoogeography of islands: the colonization of empty islands. Ecology, 50, 278-296.

Simberloff, D. & Wilson, E.O. (1970) Experimental zoogeography of islands: a two-year record of colonization. Ecology, 51, 934-937.

Wilson, E.O. & Simberloff, D. (1969) Experimental zoogeography of islands: defaunation and monitoring techniques. Ecology, 51, 267-278.

 

*Those of you who remember Current Contents will know what this means and here is the actual commentary.

Mind the gap – time to make sure that scientists and practitioners are on the same page

I have deliberately used the same title for this post as my 2017 Editorial in Annals of Applied Biology and if you were to run it through Turnitin™ you would find a very high percentage similarity indeed 🙂 I had originally planned for this post and my Editorial to appear simultaneously, but thanks to modern publishing practices, the January issue of the Annals of Applied Biology, hit the virtual newsstands in mid-December and put the kibosh on my cunning plan.

Once a year I am wheeled out to do a guest lecture to the final year agriculture undergraduates on the Global Food Production module here at Harper Adams.  I start off the lecture by reminiscing about when I was an agricultural zoology undergraduate student at the University of Leeds in 1975 and was introduced to the concept of Integrated Pest Management (IPM), or as it was termed then, Integrated Pest Control.  I was very much taken by this idea and on my next visit home, approached my Uncle James, a farmer, and explained the concept to him and suggested that he might like to implement it on his farm.  To my surprise, he was not convinced by my arguments, and replied with words to the effect, “It all sounds rather tedious, and after all, I can do all my pest control much more easily using a tank mix, so why should I bother?”.  This attitude was, at the time widespread among the UK farming community and elsewhere despite the concept having been formally discussed in the scientific literature since the late 1950s and early 1960s (Stern et al., 1959; de Fluiter, 1962).  Despite the benefits of IPM being recognised and extolled IPM by researchers and agronomists for many years, take-up by growers has been much slower than expected (Kogan, 1998; Hammond et al., 2006). Resistance to the adoption of integrated pest management is not new, Benjamin Walsh writing in 1866 wrote

“Let a man profess to have discovered some new patent powder pimperlimplimp, a single pinch of which being thrown into each corner of a field will kill every bug throughout its whole extent, and people will listen to him with attention and respect.  But tell them of any simple common-sense plan, based upon correct scientific principles, to check and keep within reasonable bounds the insect foes of the farmer, and they will laugh you to scorn”  Benjamin Walsh The Practical Entomologist

Why, if IPM is regarded as being of such paramount importance to sustainable crop production, the European Union for example passed a directive recently (2009/128/EC) requiring all member states to pass legislation to make sure that all professional growers at the very least adopt the principles of IPM, is its adoption so slow.  Hokkanen (2015) cites three main impediments to the adoption of IPM, science funding, political interference and economics.  As an applied entomologist I know from bitter experience, that there is a lack of willingness by the UK Research Councils to fund basic applied science i.e. grants to aid researchers to establish much-needed new economic thresholds are very unlikely to be funded.  Hokkanen (2015) also points out that whilst the political landscape now includes IPM, different governments have views, not necessarily based on science, about what are acceptable items for the IPM toolbox, genetically modified crops (GM) and neonicotinoid insecticides being just two such examples. Thirdly, as Hokkanen (2015) points out the ability of farmers to fully adopt IPM practices, is often out of their control, but is decided by market forces and social and political pressures, GM crops and neonicotinoids again serving to illustrate this point.

As Felicity Lawrence writing in the Guardian says “British farmers growing wheat typically treat each crop over its growing cycle with four fungicides, three herbicides, one insecticide and one chemical to control molluscs. They buy seed that has been precoated with chemicals against insects. They spray the land with weedkiller before planting, and again after.

They apply chemical growth regulators that change the balance of plant hormones to control the height and strength of the grain’s stem. They spray against aphids and mildew. And then they often spray again just before harvesting with the herbicide glyphosate to desiccate the crop, which saves them the energy costs of mechanical drying.

Most farmers around the world, whatever the crop, will turn to one of just six companies that dominate the market to buy all these agrochemicals and their seeds. The concentration of power over primary agriculture in such a small number of corporations, and their ability both to set prices and determine the varieties available, has already been a cause of concern among farmers. Yet by next year the competition is likely to shrink even further”.

Independent advice in the UK is not as easy to get as it once was.  The expected career outcome for my undergraduate course was either academia or to work as an advisor for the then, government funded, Agricultural Development and Advisory Service (ADAS).  ADAS was the research and advisory arm of the then Ministry of Agriculture Fisheries and Food and employed specialist advisers throughout the country to advise farmers and growers how to maximise their output.   ADAS became an agency in 1992, was privatised in 1997 and in December 2016 was taken over by RSK, a large environmental consultancy.  The first incarnation of ADAS was relatively well-staffed with truly independent advisors. The second incarnation, although still billed as independent, had far fewer offices and far fewer staff, so their traditional advisory role was largely taken over by private agronomists whose agendas and training are very varied.  This state of affairs is not unique to the UK.

As an example, this is from another of my correspondents who is also on the Editorial Board of Annals of Applied Biology “Thanks for your message and interesting question.  You are correct that in the US the extension service is closely aligned with the land grant Universities.  It was the complete opposite in Australia and NZ (similar to the UK) where the government funded extension service had been cut years ago and the gap had been ‘filled’ by private consultants which were also often chemical sales representatives.”

Even in the USA, traditionally very strong when it comes to entomology in universities, the situation is less than rosy as this email from another correspondent (of necessity anonymised) highlights:

“I am currently the only trained entomologist in any XX university with a position focused on commercial ornamental entomology despite nurseries in XX being our largest plant-based agricultural commodity. Between shipping out 75-80% of the nursery plants across a state or international border, thousands of cultivated varieties, several planting systems (protected and field grown), and the aesthetic thresholds with ornamental plants, I’m a bit too popular (couldn’t haven’t happened in high school when I could have used it). I don’t even have a PhD and my position is actually a regional Extension educator position versus specialist. Since we have no specialists for non-food crops, I often am asked to work off position description on other ornamental plant needs in landscapes as well. Not just entomology as this is an IPM position.  This level of demand has curtailed my ability to be involved with activities that would have been useful professionally (like publishing more and reviewing work of peers). No regrets about the new discoveries, adoption and impact of my work in many diverse areas but I will have less legacy in the published world.  

I’m retiring in less than three years. A little early but necessary as I’ve been fighting burn-out for years. And the university has taught me many times that they value my work less as a female (the stories I could tell). Women in STEM gets lots of verbiage but those of us working in these systems will tell you how far we have to go yet to be treated equitably. Perhaps they will value my work once I’m gone and people have nowhere to go. I have been fortunate to have had the privilege of excellent training and only hope that this country can maintain some of these bastions of entomology into the future”

Science is crucial to the development of IPM, be it understanding pest phenology, developing and evaluating biocontrol agents or obtaining a basic understanding of the biology and ecology of a particular pest (e.g. Webb et al., 2015; Dandurand & Knudsen, 2016; Karley et al., 2016; Rowley et al. 2016).  Basic science is important, but funding needs to be mainly allocated to more immediately applicable research than to the more academic end of the spectrum which is where it tends to go more often than not (Hokkanen, 2015).   I recently attended a conference organised by AgriNet, http://www.agri-net.net/ whose mission statement is “AGRI-net is an Agri-science Chemical Biology network which aims to stimulate the development and facilitate the translation of novel tools and technologies to key end-users in the Agri-sciences”, the title of which was  Bridging the gap between Physical sciences & Agri-sciences research.  Although the science presented was excellent it was hard to see how it could be translated to the relevant end-users in their lifetimes.

Don’t get me wrong, basic science is needed as there will be a time when the technology is available for it to be relevant.  As an example, Winer et al. (2001) convincingly demonstrated that planting spring wheat at extremely high densities (up to 600 seeds m²) in a grid pattern, significantly reduced weed density and significantly increased yield when compared with planting at conventional seed rates and in the traditional row pattern.  Fifteen years ago this may not have been very attractive to farmers as it would have meant modifying their already expensive machinery.  With the advent of precision farming this is perhaps now a viable strategy, but so far is little taken up by growers.  Is this a lack of communication from the scientists to the end-user or a reluctance to adapt new ways by the farmer?  I would suggest the former.

The recent State of Nature report (Hayhow et al., 2016) caused dismay amongst UK ecologists and raised the hackles of the UK farming community.  The data were very convincing and much of the decline in wildlife in agricultural systems was attributed to the intensification of agriculture post World War 2. The UK farming community reacted quickly and angrily (Midgely, 2016), pointing out that farming practices have changed greatly over the last half century and that the report was overlooking the many farmers who have willing engaged with the various environmental stewardship initiatives.  The debate was somewhat exacerbated by the fact that some trenchant exchanges on both sides of the fence are of a long-standing nature.  Although I have a great deal of sympathy for the conservation side of the argument I sometimes feel that the language used by what the farming press equally dismissively calls ‘green lobby’ does not help. Michael McCarthy for example, an author whom I greatly admire, is in his recent book, The Moth Snowstorm, is extremely scathing about the practices of farmers, whom he mockingly calls “Farmer Giles” (McCarthy, 2016)

Similarly, there has been for some time, a debate within the scientific community as to whether it is better to farm intensively to maximize yields while conserving and protecting natural habitats (land sparing), or to use wildlife-friendly farming methods (land sharing) that integrate biodiversity conservation with food production (e.g. Tscharntke et al., 2012; Bommarco et al., 2013; Fischer et al., 2014; Kremen, 2015).  Due, however, to the pressures imposed by academic institutions and state funding bodies, the scientists concerned publish in ‘high impact’ conservation journals unlikely to be read by agronomists let alone farmers.

Sue Hartley (2016) “…working in Malawi on a Christian Aid funded project on improving crop resilience to drought.  I thought I had the answer: farmers should stop growing maize and grow the much more drought tolerant millet instead.  Consternation amongst the farmers greeted that suggestion! “But, they exclaimed in horror, Dr Sue, we can’t we are married to maize!  Hopelessly naïve, I had neglected the wider cultural and socioeconomic context; I’d focussed on the physiology of the plants, my discipline, and not on the sociology of farmer behaviour, someone else’s discipline”

There are ways to bridge the gap, although it may mean some scientists having to step outside their laboratories and comfort zones. A recent experiment in China where academic staff and their postgraduate students lived in farming communities and worked alongside local farmers resulted in significant increases in crop yields (Zhang et al., 2016).  Whilst not suggesting that all scientists involved in basic science with potential agricultural applications, adopt a similar approach, I would encourage them to spend some time speaking to farmers on their farms and not in workshops away from the agricultural environment.   Similarly, I would exhort ecologists with an interest in agriculture to either publish in journals more likely to be read by agronomists and farmers and not in journals that only their peers will read. Arguments in journals such as Biological Conservation, no matter how well presented or reasoned, reach a very limited audience of peers and undergraduates writing assignments. The people who make the decisions and grow our food do not read those journals. Failing that, in these days of ‘research impact’ it would make sense to take steps to summarise their findings in a more popular format such as the farming press. The workshops often mentioned in grant applications under the “pathways to impact” section will only have a limited reach and the proposed web sites, another favourite of the grant writer, unless extensively advertised and scrupulously kept up to date, again will remain largely unread.

Most importantly, use language that everyone can understand.  The farmer representing Innovate UK at the Agri-futures meeting was particularly scathing about the presentations, slickly and smoothly delivered by the obviously keen and excited scientists, remarking that most farmers would not know the word heterogeneity; keep it simple, avoid jargon, but don’t speak down to practitioners just because they don’t have the same vocabulary you do.   Emma Hamer the Senior Plant Health advisor for the National Farmers Union was just one of the many speakers from industry at the Advances in Integrated Pest Management Conference that I attended in November, who pointed out that many farmers were still unaware of exactly IPM was, even though they were practicing it to some extent.

There are agricultural scientists who do their best to step down from their ivory towers and try to make their work easily accessible.  Rothamsted Research for example, where the scientists are under immense pressure to publish in high impact journals, are doing their best to provide an effective extension service despite the swingeing cuts that have been made to their staff who work with whole organisms.  Their advocacy of the IPM concept via their app Croprotect is innovative and useful.  The UK of course is not alone in these types of ventures.  My Editorial sparked this response via email:  “I read with interest your editorial in the Annals of Applied Biology.  Our research group works strongly with State Government to convert our research into practical tools for fire management, but we struggle at the interface because each agency things that it is the responsibility of the other to do the extension work!  A better example comes from my colleagues in the crop sciences who have a very workable model in the southern hemisphere (see http://www.apen.org.au/extensionnet ).” On the other hand, we have scientists who extol the virtues of extension but publish in journals that are non-accessible to many academics and certainly beyond the ken of agronomists and farmers (Kremen, 2015).  Important commentaries on pollinators aimed at farmers and politicians (Dicks et al., 2016) are too often hidden behind ‘high impact’ paywalls and if not revealed by helpful bloggers such as Jeff Ollerton, would remain hidden away from the very people who need to know.  Other bloggers such as Manu Saunders are also on the case, debunking and/or publicising the debates surrounding sustainable agriculture, but this is not enough.  Scientists who put themselves forward as working in the agricultural sciences need to pay more heed to the ways in which farmers work, understand the farming year* and actually talk to farmers whilst in their own environment.  Perhaps not so much as being on the same page but standing in the same field.

Pleased to see that a Wordle analysis of this post puts farmers centre stage.

 

References

Bommarco, R., Kleijn, D. & Potts, S.G. (2013) Ecological intensification: harnessing ecosystem services for food security. Trends in Ecology and Evolution, 28, 230–238

Dandurand, L.M. & Knudsen, G.R. (2016) Effect of the trap crop Solanum sisymbriifolium and two biocontrol fungi on reproduction of the potato cyst nematode, Globodera pallida. Annals of Applied Biology, 169, 180-189

De Fluiter, H.J. (1962) Integrated control of pests in orchards. Entomophaga, 7, 199-206.

Dicks, L.V., Viana, B., Bommarco, R., Brosi, B., del Coro Arizmendi, M., Cunningham, S.A., Galetto, L., Hill, R.,  Lopes, A.V., Pires, C., Taki, H., & Potts, S.G. (2016) Ten policies for pollinators.  Science, 354, 975-976.

Fischer, J., Abson, D.J., Butsic, V., Chappell, M.J., Ekroos, J., Hanspach, J., Kuemmerle, T., Smith, H.G. & von Wehrden, H. (2014) Land sparing versus land sharing: moving forward. Conservation Letters, 7, 149–157

Hammond, C.M., Luschei, E.C., Boerboom, C.M. & Nowak, P.J. (2006) Adoption of integrated pest management tactics by Wisconsin farmers.  Weed Technology, 20, 756-767

Hartley, S. (2016) In praise of interdisciplinarity.  The Bulletin, 47, 5-6.

Hayhow, D.B., Burns, F., Eaton, M.A., Al Fulaij, N., August, T.A., Babey, L., Bacon, L., Bingham, C., Boswell, J., Boughey, K.L., Brereton, T., Brookman, E., Brooks, D.R., Bullock, D.J., Burke, O., Collis, M., Corbet, L., Cornish, N., De Massimi, S., Densham, J., Dunn, E., Elliott, S., Gent, T., Godber, J., Hamilton, S., Havery, S., Hawkins, S., Henney, J., Holmes, K., Hutchinson, N., Isaac, N.J.B., Johns, D., Macadam, C.R., Mathews, F., Nicolet, P., Noble, D.G., Outhwaite, C.L., Powney, G.D., Richardson, P., Roy, D.B., Sims, D., Smart, S., Stevenson, K., Stroud, R.A., Walker, K.J., Webb, J.R., Webb, T.J., Wynde, R. and Gregory, R.D. (2016) State of Nature 2016. The State of Nature partnership.

Hokkanen, H.M.T. (2015) Integrated pest management at the crossroads: science, politics or business (as usual)?  Arthropod-Plant Interactions, 9, 543-545

Karley, A.J., Mitchell, C., Brookes, C., McNicol, J., O’Neill, T., Roberts, H., Graham, J. & Johnson, S.N. (2016) Exploiting physical defence traits for crop protection: leaf trichomes of Rubus idaeus have deterrent effects on spider mites but not aphids.  Annals of Applied Biology, 168, 159-172

Kogan, M. (1998) Integrated pest management: historical perspectives and contemporary developments.  Annual Review of Entomology, 43, 243-270

Kremen C. (2015) Reframing the land-sparing/land-sharing debate for biodiversity conservation. Annals of the New York Academy of Sciences, 1355, 52–76.

McCarthy, M. (2016) The Moth Snowstorm, Hodder & Stoughton, London.

Midgely, O. (2016) Industry’s work overlooked by UK green lobby. Farmer’s Guardian, September 16, 2

Rowley, C., Cherrill, A., Leather, S., Nicholls, C., Ellis, S. & Pope, T. (2016) A review of the biology, ecology and control of saddle gall midge, Haplodiplosis marginata (Diptera: Cecidomyiidae) with a focus on phenological forecasting.  Annals of Applied Biology, 169, 167-179

Stern, V.M., Smith, R.F., Van Den Bosch, R., & Hagen, K.S. (1959) The integrated control concept. Hilgardia, 29, 81-101.

Tscharntke, T., Clough, Y., Wanger, T.C., Jackson, L., Motzke, I., Perfecto, I., Vandermeer, J. & Whitbread, A. (2012) Global food security, biodiversity conservation and the future of agricultural intensification. Biological Conservation, 151, 51–59

Webb, K.M., R.M. , Harveson, R.M. & West, M.S. (2015)  Evaluation of Rhizoctonia zeae as a potential biological control option for fungal root diseases of sugar beet.  Annals of Applied Biology, 167, 75-89

Winer, J., Griepentrog, H.W. & Kristensen, L. (2001) Suppression of weeds by spring wheat Triticum aestivum increases with crop density and spatial uniformity.  Journal of Applied Ecology, 38, 784-790.

Zhang, W., Cao, G., Li, X., Zhang, H., Wang, C., Liu, Q., Chen, X., Cui, Z., Shen, J., Jiang, R., Mi, G., Miao, Y., Zhang, F. & Dou, Z. (2016) Closing yield gaps in China by empowering smallholder farmers. Nature, 537, 671-674

*As first year undergraduates, we visited the university farm once a week to do just this, even those of us doing entomology.  That experience proved invaluable, even to those of us who had worked in farms before becoming students.

A Roundabout Review of the Year – highlights from 2016

Welcome to my traditional, well it is the fourth after all, annual review of my social media and science communication activities.  I have had another enjoyable year blogging and tweeting, and as I wrote last year, I have absolutely no plans to stop either.   You may also be pleased to know that pictures of roundabouts will continue to appear at irregular intervals 🙂

Roundabout on the edge of Prades, 2016, complete with the author 🙂

 

Impact and reach

I have continued to post at about ten-day intervals; this is my 142^nd post.  The more I write the easier it seems to become. I also did my first jointly authored post, teaming up with Anne Hilborn (@AnneWHilborn) to ask if naming study animals introduced observational bias which generated a fair bit of interest and was published in a slightly modified form in the on-line magazine Biosphere.  Another of my blog articles was converted into a discussion piece for the journal Agricultural & Forest Entomology  (see February 2017 issue) and my blogging activities resulted in me being asked to do an article about roundabouts and their biodiversity for the summer newsletter of the International Association for Landscape Ecology.  For those of you who think that social media has no place in science, I feel that this is pretty convincing evidence that science communication via social media is a  very worthwhile use of our time.

I had visitors from 164 countries (150 last year) and received 34 036 views (29 385 last year).  As last year, the majority of my readers

The top ten countries for views in 2016

came form the UK and USA, although Sweden and The Netherlands made it into the top ten, pushing Spain into the wilderness.

 

Top reads

My top post (excluding my home page) in 2016 was one of my entomological classics, the Moericke Trap, closely followed by  A Winter’s Tale – Aphid Overwintering,  although my all-time winner is still Not All Aphids are Vegans with over 5 000 views.  My top ten posts tend to be either about aphids or entomological techniques/equipment which I guess means that I am filling an entomological niche.  I was however, disappointed to see that one of my favourite posts about (to me at any rate) the inspirational paper by Mike Way and Mike Cammell on using aphid egg counts to predict crop damage is languishing in the bottom ten, despite being published in September 2015 😦

 

Comparative statistics

One of the things that I find somewhat frustrating with blogging is the difficulty of gathering comparative data.  It may be the scientist in me or perhaps I am just too competitive, but as WordPress kindly supply their users with personal statistics, I feel the need to know how others are doing.  It is surprisingly hard to get these sort of data although this site is useful if you are hoping to use your blog for generating an income.  I was very excited a few weeks ago when my blog reached over 100 000 views at beginning of December.  Just a few days later Dynamic Ecology announced their 1 00 000 unique visitor which certainly put me in my place!   They have, however, been around a while and post much more frequently than I do, so are perhaps not the best yardstick, although of course something to aspire to.  Luckily, Jeff Ollerton who has been blogging about a year longer than me and in a similar subject area, is as obsessed with blogging statistics as I am and very kindly gave me access to his data.  Looking at the data it seems that we arrived at the same point

Comparative statistics between my blog and that of Jeff Ollerton’s Biodiversity Blog.

after the same amount of time but in different ways.  Jeff had a much slower start than me and his stats are best described using a curvilinear relationship whereas my line is still a straightforward linear relationship.  I guess that as I was on Twitter when I launched my blog that I immediately picked up more views than Jeff who only joined the Twitter fraternity a month or so ago.  It will be interesting to see if his readership curve steepens in the coming months and if mine continues to rise linearly, plateau or (hopefully) take-off as Jeff’s did.

Tweeting for entomology

In terms of Tweeting I had a really great experience curating the Real Scientists Twitter account @realscientists.  It kept me very busy but I interacted with a whole new set of people and had some really interesting conversations.  I can heartily recommend it to anyone who is considering volunteering.  I had hoped to hit the 5 000 follower milestone before the end of the year but didn’t quite make it, ending the year with 4 960 instead which is according to my children, pretty good for a normal person 🙂

Many thanks to all my readers and especially to those who take the time to comment as well as pressing the like button.  My top commenters, as indeed they were last year, were Emma Maund, Emily Scott, Emma Bridges, Jeff Ollerton, Amelia from A French Garden and Philip Strange.  I look forward to interacting with you all in 2017.  A Happy and Prosperous New Year to you all.