Entomological Classics – The Beating Tray or Japanese Umbrella

Southwood writing in 1966 in Ecological Methods, somewhat disparagingly refers to the beating of insects as “This is a collector’s method and originally the tree was hit sharply with a stick and the insects collected in an umbrella held upside down under the stick.” Unfortunately, he committed the cardinal sin of not supplying a supporting reference for his statement – tut, tut!  This of course set me off on one of my procrastinatory quests 🙂 Despite the fact that a certain type of beating tray is sold commercially as a Japanese umbrella I was unable to find any mention to the term in the older entomological literature.

Japanese Umbrella available from Insecta.Pro http://store.insecta.pro/catalog/2041 Also described as Clap Net (Japanese Umbrella) by a Czech company EntoSphinx http://www.entosphinx.cz/en/47-sklepavadla

Mentions to umbrellas being used to collect insects, yes, and this rather nice colour image with an umbrella shown as an essential part of an entomologist’s equipment (Schaeffer, 1766), also yes; Japanese umbrella, no.

Entomological equipment in the 18^th Century from Elementa Entomologia (1766) by Jacob Christian Schaeffer (1718-1790).

It seems that the modern beating tray is descended from two ancestors, the entomological umbrella, which judging by the earliest illustrations must have arisen sometime prior to 1766, and the clap net or clap-net, which was in use by

The entomological umbrella in use (Howard, 1910).  Note that the illustration is taken from a work by Ernest August Hellmuth von Kiesenwetter (1820-1880) which I have been unable to track down ☹

British entomologists from at least the same time (Wilkinson, 1978) and which fits in with the usage data from Collins English Dictionary.

Record of usage of the term clap-net (From Collins English Dictionary) Clap nets are used nowadays by ornithologists and bear very little resemblance to the entomological clap net but may explain the couple of more recent peaks in the usage data.

It is likely that the clap net was invented by Benjamin Wilkes possibly in the 1740s (Wilkinson, 1966) as he described how to make one.  It is interesting to see that although the clap net was used in a similar way in which we use butterfly nets today, Wilkes points out the need to have a stick with which to beat shrubs and trees to, as he puts it “wherewith to put the flies and moths on the wing”

The clap net in butterfly net mode (Wilkinson, 1966)

Here Newman (1835) highlights the use of the clap net as a beating tray

The clap net (circled) and other entomological equipment, from Ingpen (1849). Note the resemblance to a beating tray.

Ingpen (1849) in his description of the use of the clap net specifically mentions its use as a beating tray “When beating into the net, it will be necessary to keep both sticks in the left hand*, at the same time keeping the head of the net as wide open as possible”.  This pretty much how I use my rathe superior(and expensive) beating tray 😊 We then get a mention of the entomological umbrella “In the absence of a clap-net, an open umbrella, will in general be found convenient for beating into; particularly if the inside be lined with white cotton and made to cover the whalebone”. It seems that the umbrella as a beating tray was in common use by the middle of the nineteenth century, for example, “these may be captured by beating the branches over a large net or umbrella” (Douglas & Scott, 1865).  This is not to be confused with the beating-net which was an early name for the sweep net (Packard, 1873), the history and use of which I have written about earlier.

So when do beating trays become recognised as beating trays? Banks (1909) refers to both the umbrella, incidentally also using the Keisenwetter illustration, but comments that “A substitute for the umbrella, and in many cases better than it, is the beating cloth. It consists of a piece of common unbleached cot- ton cloth, 1 yard square, to each corner of which a loop of stout twine is sewed, or a corner turned over. Upon reaching the woods, two straight sticks, each about 5 feet in length, and not too heavy, also not so small as to break or bend too easily, are cut from a convenient bush. The sticks are placed crosswise over the cloth and fastened to the loops at the four ends. This is easily and quickly done by making sliding loops of the simple loops. The cloth is thus kept spread out between the sticks. To the center of the sticks another stick may be fastened, so as to hold the cloth out under the branch.”  George Day in his 1916 Presidential address to the Entomological Society of British Columbia refers to umbrellas and beating trays in the same sentence “Another method is by beating the foliage of trees and shrubs over a beating tray or inverted umbrella” (Day, 1918). Given that the biologist and novelist, Elliot Grant Watson (1885-1970) refers, somewhat caustically, to beating trays in his essay published in The English Review  “Enthusiastic entomologists smashing the young buds from the bushes, holding out beating trays” (Watson, 1923), I am failry confident that the beating tray as we know it, had replaced umbrellas, entomologcial or otherwise, by about 1920. I have still to find out where the term “japanese umbrella” arose.  Let me know in the comments if you are able to help.

My modern beating tray – costs about twice as much as the Japanese Umbrella, modern clap net or collapsible beating tray.

Modern beating tray in use – more like the original entomological umbrella depicted by Howard (1910), albeit I am somewhat stouter than the entomologist in his illustration.

References

Banks, N. (1909) Directions for Collecting and Preserving Insects.  United States National Museum Bulletin 67, Smithsonian Institute, Washington.

Day, G.O. (1918) Larva rearing.  Journal of the Entomological Society of British Columbia, 8, 21-27.

Douglas, J.W. & Scott, J. (1865) The British Hemiptera, Volume 1, Hemiptera-Heteroptera. Ray Society, London.

Howard, L.O. (1910) The Insect Book. A popular account of the bees, wasps, ants, grasshoppers, flies and other North American insects exclusive of the butterflies, moths and beetles, with full life histories, tables and bibliographies. Doubleday, Page & Company, New York, xxvii + 429 pp.

Ingpen, A. (1849)  Manual for the Butterfly Collector or instructions for Collecting, Rearing and Preserving British and Foreign Insects. David Bogue, London.

Newman, E. (1835) The Grammar of Entomology. Frederick Westley & A. H. Davis, London

Packard, A.S. (1873) Directions for Collecting and Preserving Insects. Smithsonian Miscellaneous Collections 261, Washington.

Watson, E.L.G. (1923) The New Forest, The English Review (September), 318-320

Wilkinson, R.S. (1966) English entomological methods in the seventeenth and eighteenth centuries II: Wilkes and Duffield. Entomologist’s Record and Journal of Variation, 78, 285-292.

Wilkinson, R.S. (1978) The history of the entomological clap-net in Great Britain. Entomologist’s Record and Journal of Variation, 90, 127-132.

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Were all Victorian entomologists right-handed?  I think not 😊. Though that said, even as recently as my mother’s and father’s generation (born in the 1920s) left-handed children were often forced to use their right hands.

Entomological classics – Aphids spit: visualising aphids feeding, the electrical penetration graph

Aphids as a taxonomic group, have been recognised since at least 1758 when Linnaeus coined the genus Aphis and have been cited as important pests for more than 200 years “The Aphis or Blighter, as we now for the first time venture to call it, from its being the most general cause of what are termed blights in plants..” (Curtis, 1802).  A detailed understanding of how they fed, was however, longer in being reached, but by 1914 the anatomy of the aphid mouthparts and the process of stylet insertion was fully described (Davidson, 1914).  Davidson (1923) also described the role that aphid saliva plays in helping the aphid feed by making it easier for the stylet to move between cells on its convoluted journey to the phloem, made visible as the so-called stylet tracks.

Drawings showing the effects produced by the passage of aphid stylets of three different aphid species through leaf tissue (Davidson, 1923).

Fast forward a couple of years and we have intrepid entomologists producing photographic evidence of aphid stylets in action (Smith, 1926).

Photomicrographs of the stylet of Myzus persicae in situ and the resultant stylet track (Smith, 1926).

One of the reasons that applied entomologists were so interested in aphid feeding was the role that aphids, and other insects, played as vectors of plant viruses, which until the 1920s, was not formally proven (e.g. Kunkel, 1926, Smith, 1926, 1929). You would be forgiven for thinking that once the connection between aphid feeding and plant virus transmission had been demonstrated then that would be it.  But no, much wants more, and aphidologists became intrigued about the link between aphid feeding and salivation, in particular when and exactly where these activities occurred in the plant.  Those entomologists working on plant viruses wanted to know which part of the feeding process was linked to the acquisition and inoculation of the viruses from and to the aphid host plant.  A possible solution to these conundrums, was, however, on the horizon.

In the early 1960s, two entomologists from the Department of Entomology, at the University of California, Davis, Donald McLean and Marvin Kinsey,  came up with a system that was to revolutionise the study of the feeding behaviour of aphids and other insects that feed internally on plant using piercing mouthparts (McLean & Kinsey, 1964). In essence, what they did was to make an aphid part of an electrical circuit by attaching a thin copper wire to its back using a quick-drying silver paint.  The feeding substrate, a leaf, had a 2.0 Volt, 60-cycle alternating current introduced to it and this was placed on an insulated grid connected to an amplifier connected in parallel with an oscilloscope, a chart-recorder and a speaker. The wire attached to the aphid, was joined to the grid and when the aphid began to feed this completed the circuit, and changes in voltage were able to be observed and recorded.  The next step was to identify which chart recordings were associated with sap ingestion and salivation by the aphid.  Using an artificial leaf, Parafilm stretched over a well containing a sucrose solution, and watching the aphids under a high power microscope, these innovative entomologists were able to identify four different stages involved in aphid feeding (Mclean & Kinsey, 1965).

The ground-breaking chart recording (Mclean & Kinsey, 1965) and as you might expect it was a pea aphid 🙂

 

A visual summary of what McLean and Kinsey were watching and recording (from Dixon (1973).

Not satisfied with these findings McLean and Kinsey modified their equipment and intensified their observations, sacrificing a number of aphids in the process.  When different waveforms were seen the poor aphids had their stylets amputated and the plant material with the stylet still in place was then examined under a high power microscope.  This meant that they were able to definitively correlate their recordings with the position of the stylet in different leaf tissues and during different behaviours (McLean & Kinsey, 1967).  As well as trying to understand how, when and where plant viruses were acquired or transmitted, it turns out that using the waveforms generated by the aphid mouthparts as they weave their way through the leaf tissues, is not only a useful way of assessing the resistance mechanism of a plant (e.g. Nielson & Don, 1974; Paul et al., 1996; ten Broeke et al., 2016) but also for detecting resistance to insecticides (e.g. Garzo et al., 2016).

Modifications to the original equipment happened very quickly; by 1966, a more compact and easier to use version using Direct Current had been developed (Schaefers, 1966). That said, the first correlation of a specific waveform and virus acquisition by the pea aphid, was shown using the original AC equipment (Hodges & Mclean, 1969).  A further modification of the Schaefers DC equipment was developed during the 1970s, such that test aphids were able to live and reproduce for up to ten days whilst attached to the set-up, thus allowing very detailed investigation of the correlations between the electrical signal patterns produced and the feeding behaviours of the aphids (Tjallingii, 1978).

Those of you who take note of such things, will have noticed, that so far, some 14-years after its invention, the term electrical penetration graph has not yet appeared, either here or in the scientific literature.   Earlier references to recordings using the technique use the term actograph which was somewhat non-specific, as it refers to any graphical representation of behavioural activity.  So when did the term Electrical Penetration Graph (EPG) first appear in the literature.  Google Scholar gave me a date of 1984 from a paper looking at the resistance of lettuce to the cabbage aphid Brevicoryne brassicae, a paper that includes Freddy Tjallingii in the authorship list (Mentink et al., 1984).  In this paper the authors refer to a conference proceedings paper (Tjallingii, 1982) as being the source of the name.  On tracking down that paper I found that it doesn’t actually mention the term EPG.  The first paper that specifically mentions and defines the term as “the recorded graph as a result of an overall electrical signal caused by stylet penetration activities” is Tjallingii (1985).  Strangely the author introduces the term thus “Here we introduce the term ‘electrical penetration graph (EPG)”, which I found slightly odd as it is a single author paper 😊  Inputting EPG or electrical penetration graph into Web of Science shows an increasing number of papers using and mentioning the technique, but surprisingly the first paper recorded is from 1999.

NGram finds the first mention slightly earlier, 1981.  A puzzle waiting to be solved for anyone with the time or inlcination.

The frequency of the occurrence of the phrase “Electrical penetration graph” according to Ngram Viewer (accessed and downloaded May 1^st 2018).

The technique is now very well established and used around the world.  The equipment is commercially available through EPG Systems, which is where we got ours from and just in case you were wondering, this is what it looks like.

Faraday Cage (an earthed metal screen) surrounding the equipment to exclude electrostatic and electromagnetic influences

Our test plants in situ connected up to the electrical supply, recording equipment and amplifier.

Close up of the plants and EPG electrodes

Aphids connected up to the EPG. Photo courtesy of https://sites.google.com/site/ezwear1/epgIMG_0903.jpg

A simple guide to interpreting the waveforms

http://www.epgsystems.eu/file/46-waveform-features

For Open Days and public displays it is not unknown for mischievous entomologists to link particular waveforms to recordings of sucking and spitting sounds and to play these back when the equipment is being demonstrated 🙂

 

References

Curtis, W.L. (1802) IV. Observations on aphides, chiefly intended to show that they are the principal cause of blights in plants, and the sole cause of the honeydew.  Transactions of the Linnaean Society of London, 6, 75-94.

Davidson, J. (1914) On the mouth-parts and mechanism of suction in Schizoneura lanigera, Hausmann. Zoological Journal of the Linnaean Society, 32, 307-330.

Davidson, J. (1923) Biological studies of Aphis rumicis Linn. The penetration of plant tissues and the source of the food supply of aphids.  Annals of Applied Biology, 15, 35-54.

Gabrys, B., Tjallingii, W.F. & van Beek, T.A. (1997) Analysis of EPG recorded probing by cabbage aphid on host plant parts with different glucosinolate contents. Journal of Chemical Ecology, 23, 1661-1673.

Garzo, E., Moreno, A., Hernando, S., Marino, V., Torne, M., Santamaria, E., Diaz, I. & Fereres, A. (2016) Electrical penetration graph technique as a tool to monitor the early stages of aphid resistance to insecticides. Pest Management Science, 72, 707-718.

Hodges, L.R. & McLean, D.L. (1969) Correlation of transmission of Bean Yellow Mosaic Virus with salivation activity of Acyrthosiphon pisum (Homoptera: Aphididae). Annals of the Entomological Society of America, 62, 1398-1401.

Kunkel, L.O. (1926) Studies on Aster Yellows. American Journal of Botany, 13, 646-705.

McLean, D.L. & Kinsey, M.G. (1964) A technique for electronically recording aphid feeding and salivation. Nature, 202, 1358-1359.

McLean, D.L. & Kinsey, M.G. (1965) Identification of electrically recorded curve patterns associated with aphid salivation and ingestion. Nature, 205, 1130-1131.

McLean, D.L. & Kinsey, M.G. (1967) Probing behavior of the pea aphid, Acyrthosiphon pisum. I. Definitive correlation of electronically recorded waveforms with aphid probing activities.  Annals of the Entomological Society of America, 60, 400-405.

Mentink, P.J.M., Kimmins, F.M., Harrewijn , P., Dieleman, F.L., Tjallingii, W.F.,  van Rheenen, B. &  Eenink, A.H. (1984)  Electrical penetration graphs combined with stylet cutting in the study of host plant resistance to aphids. Entomologia experimentalis et applicata, 35, 210-213.

Nielson, M.W. & Don, H. (1974) Probing behaviour of biotypes of the spotted alfalfa aphid on resistant and susceptible and alfalfa clones.  Entomologia experimentalis et applicata, 17, 477-486.

Paul, T.A., Darby, P., Green, C.P., Hodgson, C.J. & Rossiter, J.T. (1996) Electrical penetration graphs of the damson-hop aphid, Phorodon humuli on resistant and susceptible hops (Humulus lupulus).  Entomologia expeimentalis et applicata, 80, 335-342.

Powell, G. (1991) Cell membrane punctures during epidermal penetrations by aphids: consequences for the transmission of two potyviruses. Annals of applied Biology, 119, 313-321.

Schaefers, G.A. (1966) The use of direct current for electronically recording aphid feeding and salivation. Annals of the Entomological Society of America, 59, 1022-1024.

ten Broeke, C.J.M., Dicke, M. & van Loon, J.J.A. (2016) Feeding behaviour and performance of Nasonovia ribisnigri on grafts, detached leaves, and leaf disks of resistant and susceptible lettuce.  Entomologia experimentalis et applicata, 159, 102-111.

Tjallingii, W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia experimentalis et applicata, 24, 521-530.

Tjallingii, W.F. (1982) Electrical recording of aphid penetration. [In] J.H. Visser & A.K. Minks (eds.) Proceedings of the 5^th Symposium on Insect Plant-Relationships, 1-4 March, 1982, Wageningen, Pudoc, pp 409-410.

Tjallingii, W.F. (1985) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia experimentalis et applicata, 38, 177-185.

Smith, K.M. (1926) A comparative study of the feeding methods of certain Hemiptera and of the resulting effects upon the plant tissue, with special reference to the potato plant. Annals of Applied Biology, 13, 109-139.

Smith, K.M. (1929) Studies on potato virus diseases, V. Insect transmission of potato leaf roll.  Annals of Applied Biology, 16, 209-229

 

Entomological classics – The D-Vac, Vortis and other motorised suction samplers

I think that all field entomologists of a certain age, certainly those of us over 60, are very familiar with the roar of a hot and smoky two-stroke engine in our ears, coupled with oily hands, aching shoulders and sometimes the smell of burning.  Some younger entomologists may also have had this joyful experience but I suspect they are in a minority among their peers.  The dreaded D-Vac, or to give it its more formal name, The Dietrick Vacuum Sampler was, for a long time, the entomological gold standard in the world of motorised insect sampling.

Part of the UEA cereal aphid research group demonstrating unsafe use of the D-Vac 😊

The D-Vac was the brain wave of an American entomologist Everett Dietrick, who at the time was working on the biological control of the alfalfa aphid, Therioaphis maculata (Dietrick et al., 1959). Their research was hampered by the time they were having to spend estimating the numbers of all the arthropods found in alfalfa fields; they needed a standard sampling method that would allow them to get good estimates of everything rather than using different, and thus time-consuming, methods for each arthropod group.  Essentially, think of a D-Vac as motorised sweep net.  The idea of replacing sweep netting with, in theory at any rate, a non-human biased method* was not new.  Hills (1933) in describing a motorised vacuum pipette for sampling leaf hoppers in beet points out that it is an adaptation of a device put together by a lab assistant in 1926.

The first motorised suction sampler? From Hills (1933) – The modified pipette collector

The first and even clumsier model of the D-Vac (Dietrick et al., 1959), but I suspect more pleasant to use than the back-pack version 🙂

The new improved back-pack version (Dietrick, 1961).  In my experience not very comfortable and on one occasion burst into flames while I was wearing it!

This could, with the aid of a handy pole be used to sample from the top of tall bushes. Not something I have tried so I can’t comment.

While searching for the earliest reference to a motorised suction device that was not a Pooter, I came across one invented a few years earlier than the D-Vac and used by the late, great Southwood of Ecological Methods fame among others, during his PhD (Southwood, 1955; Johnson et al., 1955), which I guess means that it was in operation well before 1955, although the actual full description was not published in a journal until a couple of years later (Johnson et al., 1957).

An earlier suction device used by the late great Southwood during his PhD (1955) (From Johnson et al., 1957).

Ensuring constancy of sample area (From Johnson et al., 1957)

It really does look like the vacuum cleaner we had when I was a kid 🙂

Amusingly, one of the early attempts to replace the D-Vac was actually based on this very vacuum cleaner (Arnold et al., 1973)

I was interested to see that the Johnson apparatus used a barrel to delineate the sample area, something advocated by my colleague Andy Cherrill (Zentane et al., 2016) when using his patent G-Vac, or “Chortis” as we jokingly call it 🙂

A couple of years after I started at Silwood Park and became involved in running the final year field course, a new and revolutionary insect suction sampler appeared on the market – The Vortis™ (Arnold, 1994).  This was lighter than the D-Vac, did not need a bag or net, easier to start, had an ‘idle’ function and mercifully did not have to be carried on your back 🙂

The Vortis™, overall a much pleasanter way to sample insects and generally much easier to start.  Invented in 1993 (Arnold, 1994).

 

Although not cheap, it was less expensive than the D-Vac. This became my suction sampler of choice although we kept our D-vac in good running order so that the students could compare the two samplers.  Surprisingly, few, if any, of the many users of The Vortis™ have done similarly, most just referring to the original description by Arnold (1994), e.g. Mortimer et al., (2002).  This is in marked contrast to the many studies that have compared the D-Vac with sweep-netting, pitfall trapping and swish net sampling (e.g. Johnson et al., 1957; Henderson & Whittaker, 1977; Hand, 1986; Schotzko & O’Keeffe, 1989; Standen, 2000; Brook et al., 2008). There is also a hand-held version of the D-Vac if anyone wants to compare that with the back-pack version.

Jan Dietrick poses with a D-Vac insect Vacuum in Ventura, Calif., on Monday, Oct. 16, 2006. (Photo by Bryce Yukio Adolphson/Brooks Institute of Photography ©2006) http://bryceyukioadolphson.photoshelter.com/image/I0000pmiujJcoGBI

This one looks easier to use than the backpack version but I have never seen it in operation. I am guessing that this was produced in response to the invention of the Vortis™.

Entomologists tend to have limited budgets when it comes to equipment, or anything for that matter, so it is not surprising that they soon came up with the idea of adapting garden leaf blowers into lightweight, inexpensive insect suction samplers (e.g. De Barro, 1991; Stewart & Wright, 1995). These are collectively known as G-Vacs (Zentane et al., 2016) presumably as a reference to their garden origin.

Andy Cherrill test driving his “Chortis” 🙂

 

My colleague Andy Cherrill has compared the catch composition of his own particular G-Vac with that of the Vortis™ and satisfied himself that it is as good as, if not better than the Vortis™ (Cherrill et al., 2017).  Importantly the cost of a G-Vac means that you can get, at least in the UK, six for the same price as a single Vortis™.

I leave you with two fun facts; the two largest motorised insect suction samplers that I have come across are both from the USA (where else?).  The first, mounted on the front of a truck, was used to collect parasites for the biological control of alfalfa aphids.

(1957) http://www.dietrick.org/articles/deke_truckvac.html  Used to collect parasites for mass release against alfalfa aphids.

 

The second, mounted on the front of a tractor was used to control Lygus bugs in strawberry fields in California (Pickel et al., 1994).  The driver/operator in the second example seems to be taking Health & Safety issues a bit more seriously than the team in the first 🙂

Lygus bug control in strawberries, California http://calag.ucanr.edu/Archive/?article=ca.v049n02p19

 

References

Arnold, A.J. (1994) Insect suction sampling without nets, bags or filters. Crop Protection, 13, 73-76.

Arnold, A.J., Needham, P.H. & Stevenson, J.H. (1973) A self-powered portable insect suction sampler and its use to assess the effects of azinphos methyl and endosulfan on blossom beetle populations on oil seed rape. Annals of Applied Biology, 75, 229-233.

Brook, A.J., Woodcock, B.A., Sinka, M. & Vanbergen, A.J. (2008) Experimental verification of suction sampler capture efficiency in grasslands of differing vegetation height and structure. Journal of Applied Ecology, 45, 1357-1363.

Cherrill, A.J., Burkhmar, R., Quenu, H. & Zentane, E. (2017) Suction samplers for grassland invertebrates: the species diversity and composition of spider and Auchenorrhyncha assemblages collected with Vortis (TM) and G-vac devices. Bulletin of Insectology, 70, 283-290.

De Barro, P.J. (1991) A cheap lightweight efficient vacuum sampler.  Journal of the Australian Entomological Society, 30, 207-20.

Dietrick, E.J. (1961) An improved backpack motor fan for suction sampling of insect populations.  Journal of Economic Entomology, 54, 394-395.

Dietrick, E.J., Schlinger, E.I. & van den Bosch, R. (1959) A new method for sampling arthropods using a suction collecting machine and modified Berlese funnel separator.  Journal of Economic Entomology, 52, 1085-1091.

Dietrick. E. J., Schlinger. E. I. & Garber, M. J. (1960). Vacuum cleaner principle applied in sampling insect populations in alfalfa fields by new machine method. California Agriculture January 1960, pp. 9-1 1

Doxon, E.D., Davis, C.A. & Fuhlendorf, S.D. (2011) Comparison of two methods for sampling invertebrates: vacuum and sweep-net sampling. Journal of Field Ornithology, 82, 60-67.

Hand, S.C. (1986) The capture efficiency of the Dietrick vacuum insect net for aphids on grasses and cereals. Annals of Applied Biology, 108, 233-241.

Henderson, 1. F. & Whitaker, T. M. (1977). The efficiency of an insect suction sampler in grassland. Ecological Entomology 2, 57-60.

Hills, O.A. (1933) A new method for collecting samples of insect populations.  Journal of Economic Entomology, 26, 906-910.

Johnson, C.G., Southwood, T.R.E. & Entwistle, H.M. (1955) A method for sampling arthropods and molluscs from herbage by suction.  Nature, 176, 559.

Johnson, C.G., Southwood, T.R.E. & Entwistle, H.M. (1957) A new method of extracting arthropods and molluscs from grassland and herbage with a suction apparatus.  Bulletin of Entomological Research, 48, 211-218.

Mortimer, S.R., Booth, R.G., Harris, S.J. & Brown, V.K. (2002) Effects of initial site management on the Coleoptera assemblages colonising newly established chalk grassland on ex-arable land. Biological Conservation, 104, 301-313.

Pickel, C., Zalom, F.G.,  Walsh, D.B. & Welch, N.C. (1994) Efficacy of vacuum machines for Lygus Hesperus (Hemiptera: Miridae) control in coastal California strawberries. Journal of Economic Entomology, 87, 1636-1640.

Schotzko, D.J. & O’Keeffe, L.E. (1989) Comparison of sweep net., D-Vac., and absolute sampling., and diel variation of sweep net sampling estimates in lentils for pea aphid (Homoptera: Aphididae)., Nabids (Hemiptera: Nabidae)., lady beetles (Coleoptera: Coccinellidae)., and lacewings (Neuroptera: Chrysopidae). Journal of Economic Entomology, 82, 491-506.

Southwood, T.R.E. (1955). Some Studies on the Systematics and Ecology of Heteroptera.—Ph.D. thesis, University of London.

Standen, V. (2000) The adequacy of collecting techniques for estimating species richness of grassland invertebrates. Journal of Applied Ecology, 37, 884-893.

Stewart, A.J.A. & Wright, A.F. (1995) A new inexpensive suction apparatus for sampling arthropods in grassland.  Ecological Entomology, 20, 98-102.

Zentane, E., Quenu, H., Graham, R.I. & Cherrill, A.J. (2016) Suction samplers for grassland invertebrates: comparison of numbers caught using Vortis^™ and G-vac devices.  Insect Conservation & Diversity, 9, 470-474.

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I am sure that many of you have heard the phrase “it’s all in the wrist” when on your ecology/entomology field course and having sweep netting demonstrated to you 😊

Entomological classics – the sweep net

I am certain that everyone who has studied biology at university and/or been on a field course, will have used a sweep net and heard the phrase “It’s all in the wrist”.  Along with the pitfall trap it is the most commonly used entomological sampling technique used today.  Although the premise is simple enough, a sturdy net, attached to a handle that is swept along, through or above low-lying vegetation, when used as a scientific tool and not just as a collecting device, things become somewhat more complex.  The sweep net, as an insect collecting device, has been around for at least 180 years, the earliest reference that I have been able to find being Newman* (1835).  There are a number of slightly later references in both general entomology texts and group specific books (e.g. Newman, 1844; Clark, 1860; Douglas, 1860; Douglas & Scott, 1865). Instructions for their use at this time are minimal, as this extract from Newman (1841) illustrates.

Newman (1841) a very brief description indeed.

This slightly later description of how to make a sweep net is, however, much more detailed, albeit somewhat sexist.

From Stainton (1852), although he seems to be quoting Newman.  Apparently Victorian men were unable to sew.

More detailed, albeit fairly basic instructions on how to use a sweep net can be found in those two invaluable sources, Ecological Methods (Southwood & Henderson 2004) (two pages) and Practical Field Ecology (Wheatear et al., 2011) (one page).  I was amused to see that the text in Southwood & Henderson was identical to that of the first edition (Southwood, 1966).

Now we come to the wrist action. There are a surprising number of ways in which you can swing a sweep net, but they all depend on the wrist moving your hand, and hence the net, in a figure of eight. The two most commonly used are what I think of as the one row side step, and the double front step.  In the former you walk in a straight line swinging the net backwards and forwards at your side, ideal for sampling a row crop. The latter, the double front step, is similar, but instead of swinging the net at your side, you swing it side to side in front of you as you walk along.  In a crop, this is great for sampling multiple rows, in a non-crop a good way of covering a nice wide area of vegetation. There are a further two techniques specifically designed for sweeping the upper part of vegetation, both originally devised for sampling soybean insects, the lazy-8 and the pendulum (Kogan & Pitre, 1980).  Both these involve having the net raised, the lazy-8 with the net raised above the crop at the back and front swings, whereas in the pendulum, the net is kept within the crop on the fore and reverse swings.  The final bit of wrist action, and arguably the most important and difficult to learn, is the flick-lock, which neatly seals the net and stops your catch escaping.

Having completed your sample of however many sweeps (remember a complete sweep is the figure of eight), and sealed your net, the next step is to transfer your catch to your collecting tubes, bags or jars.  A good sweep net, as well as being made from tough material, should be a bit sock shaped.  By this I mean that there is a ‘tail’ at the base of the net which helps make your catch more manageable if you are transferring directly to a plastic bag, as you are able to grab the net above the ‘tail’ end and push it into the collecting bag, before everting the net.

Two examples of sweep nets, a large and a small one.  You can also get a medium one in this series supplied by the NHBS web site for about £34. http://www.nhbs.com/professional-sweep-net

When I was a student, the sweep nets we were supplied with, were large enough to stick not just your head inside, but also to get your arms in, so that you could Poot up anything interesting, your shoulders forming the seal to the net.  Admittedly you did sometimes have an angry bee or wasp to contend with, but that was a rare event 🙂  Nowadays, sweep nets seem to be constructed on a much more modest scale, which makes sticking your head, let alone your shoulders into one, somewhat difficult.

Even the biggest modern one is too small for me to get my arms in to do some Pooting.

I was pleasantly surprised on an ERASMUS exchange visit to the University of Angers a few years ago, to find that the French, or at least those in Angers, were using sweep nets that were big enough for me to actually delve inside just as I did when I was a student 🙂

The joys of a sweep net with a view 🙂

Despite their undoubted popularity, value for money and relative ease of operation, there are a number of problems associated with sweep netting as a sampling technique.  Although these problems are summarised elsewhere (Southwood & Henderson 2004; Wheater et al., 2011) I can’t resist putting my own personal slant on the subject.

• The type of habitat can have a marked effect on what you catch. Not all habitats are equally amenable to sweeping; spiny and woody vegetation poses more problems than a nice meadow and you need a really tough net for moorlands 🙂
• A sweep net doesn’t necessarily give you an accurate picture of the species composition of the habitat. Not all insects are equally catchable, you are for example, much more likely to catch Hemipterans than you are Coleopterans (e.g. Standen, 2000)
• The vertical distribution of the insects also affects what you catch. Many insects have favourite positions on plants e.g. the cereal aphid, Sitobion avenae prefers the ears and leaves, whereas the bird cherry-oat aphid, Rhopalosiphum padi is usually found at the bottom of the plant (Dean, 1974).
• The weather; anyone who has tried sweep netting during, or after, a rain storm knows that this is the ultimate act of folly 🙂 Wet nets and wet samples are not a marriage made in heaven.
• Time of day can also affect what you are likely to catch, pea aphids for example, are found at different heights on their host plants at different times of day (Schotzko & O’Keeffe, 1989). To be fair, this is of course not just a problem confined to sweep net sampling.
• Sweep nets have a fairly well-defined height range at which they work best, they are not good at sampling very short grass and once the vegetation gets over 30 cm you start to miss a lot of the insects associated with it as the net doesn’t reach that far down. Also the efficiency of the sweep netter is reduced.
• Finally, how the hell do you standardise your sweeps, not only between sweepers, but as an individual? Additionally, can you reliably use them quantitatively? This has been recognised as a problem for a long time (DeLong, 1932).  No one disagrees that sweep netting, provided all the caveats listed above are taken into account, gives a very good qualitative and comparative idea of the arthropod community of the area you are sweeping and they have been so used in many important ecological studies (e.g. Menhinick, 1964; Elton, 1975; Janzen & Pond, 1975) and extensively in agricultural systems (e.g. Free & Williams, 1979; Kogan & Pitre, 1980).  Comparing any sampling technique with another is difficult, and any attempt to quantify a catch so that specific units can be assigned to the area or volume sampled is welcome.  This has been attempted for the sweep net (Tonkyn, 1980), although I confess that I have never seen anyone use the formula developed by him.  In fact, although, according to Google Scholar his paper has been cited thirteen times, only one of the citing authors actually uses the formula, the rest just use him to cite sweep netting as a sampling method. Poor practice indeed.

An illustration of how the various components of the sweep net volume formula is derived (from Tonkyn, 1980).

Sweep nets are, despite the inability to get inside them anymore, great fun to use, extremely good at collecting material for ecology and entomology practicals and of course, a great ecological survey tool when used properly.  Google Scholar tells me that there are over 38 000 papers that mention them.  That many people can’t possibly be wrong 🙂

References

Clark, H. (1860) Catalogue of the Collection of Halticidae in the British Museum. Physapodes and Oedipodes Part 1. Published by the Trustees, London.

Dean, G.J. (1974) The four dimensions of cereal aphids. Annals of Applied Biology, 77, 74-78.

DeLong, D.M. (1932) Some problems encountered in the estimation of insect populations by the sweeping method.  Annals of the Entomological Society of America, 25, 13–17.

Douglas, J.W.  (1856) The World of Insects: A Guide to its Wonders. John van Voorst, London.

Douglas, J.W. & Scott, J. (1865) The British Hemiptera Volume I Hemiptera – Heteroptera. Ray Society, Robert Hardwicke, London.

Elton, C.S. (1975) Conservation and the low population density of invertebrates inside neotropical rain forest.  Biological Conservation, 7, 3-15.

Free, J.B. & Williams, I.H. (1979) The distribution of insect pests on crops of oil-seed rape (Brassica napus L.) and the damage they cause. Journal of Agricultural Science, 92, 139-149.

Janzen, D.H. & Pond, C.M. (1975) A comparison, by sweep sampling, of the arthropod fauna of secondary vegetation in Michigan, England and Costa Rica. Transactions of the Royal Entomological Society of London, 127, 33-50.

Kogan, M. & Pitre, H.N. (1980) General sampling methods for above-ground populations of soybean arthropods. Pp 30-60 [In] Sampling Methods in Soybean Entomology. (Eds.) M. Kogan & D.C. Herzog, Springer, New York.

Menhinick, E.F. (1964) A comparison of some species-individuals diversity indices applied to samples of field insects. Ecology 45, 859-861.

Newman, E. (1844) The Zoologist. A Popular Miscellany of Natural History, Volume 2. John van Voorst, London.

Newman, E. (1841) A Familiar Introduction to the History of Insects. John van Voorst, London.

Newman, E. (1835) The Grammar of Entomology. Frederick Westley & A.H. Davis, London.

Schotzko, D.J. & O’Keeffe, L.E. (1989) Comparison of sweep net., D-Vac., and absolute aampling., and diel variation of sweep net sampling estimates in lentils for pea aphid (Homoptera: Aphididae)., Nabids (Hemiptera: Nabidae)., lady beetles (Coleoptera: Coccinellidae)., and lacewings (Neuroptera: Chrysopidae). Journal of Economic Entomology, 82, 491-506.

Southwood, T.R.E. (1966) Ecological Methods, Methuen & Co., London.

Stainton, H.T. (1852) The Entomologist’s Companion; Being a Guide to the Collection of Microlepidoptera and Comprising a Calendar of the British Tineidae. John van Voorst, London.

Standen, V. (2000) The adequacy of collecting techniques for estimating species richness of grassland invertebrates.  Journal of Applied Ecology, 37, 884-893.

Tonkyn, D.W. (1980) The formula for the volume sampled by a sweep net.  Annals of the Entomological Society of America, 73,452-454.

Wheater, P.C., Bell, J.R. & Cook, P.A. (2011) Practical Field Ecology: A Project Guide, Wiley-Blackwell, Oxford.

 

*Of interest to me, but perhaps not to my readers, Edward Newman was one of the founder members of the oldest and most exclusive, yet low-key, entomological society in the world, The Entomological Club, of which I have the honour of being a member 😊 https://en.wikipedia.org/wiki/Edward_Newman_(entomologist)  founder member of the Entomological Club

 

 

Ten papers that shook my world – Solomon (1949) – quantifying predator efficiency

Solomon, M. E. (1949). The natural control of animal populations. Journal of Animal Ecology, 18, 1-35.*

 

According to Google Scholar there are 1149 (only 773 in 2013)citations to this paper, an average of 17.1 citations per year, compared with the 12.5 I reported back in 2013.  Although influential, it had a slow start, only 383 citations being recorded for it between 1949 and 1993. Since 2000 it has averaged about 48 citations a year (760 in total), 225 of those since 2013.** To the modern reader this paper comes across as wordy and discursive, more like a popular article than a scientific paper. This does not, however, mean that the science and the man behind the article were not first class. Journals had less pressure on their space in those days and scientists had more time to think and read. If only it were so now. Despite the relatively low number of citations, this paper has had an immense influence on the study of population dynamics, although I will have to confess, that for my generation who were undergraduates in the 1970s, Solomon’s little Study in Biology*** book, Population Dynamics, published in 1969, was our main, if not only, encounter with his work.

Making sure that nobody could claim my copy of Population Dynamics

Here Solomon introduces the term functional as in a density related response

Nowadays we remember the paper as the first one to formalise the term ‘functional response’ although the early citations to this paper are in reference to density dependence, competition, population regulation and population variability e.g. (Elton 1949; Glen 1954; Southwick 1955; Bakker 1963). Interestingly, one of the earlier papers to cite Solomon, (Burnett 1951) presented functional response curves but did not mention the term (Watt (1959)). To add further insult to injury, Holling (1959) in the same year, in his classic paper in which he described and numbered the types of functional responses did not even refer to Solomon, rather deferring to Watt’s paper (loc. cit.). Since then, with the likes of Varley, Gradwell and Hassell (1973) and luminaries such as Bob May (May 1978), this paper has been cited often, and justifiably, and continues to influence us to this day, including the author of this eulogy (Aqueel & Leather 2012). This paper as well as being  the first one to formalise the term ‘functional response’ was the first attempt to draw together the disparate conceptual strands of the first half of the twentieth century work on population dynamics in one coherent whole. Truly, a remarkable and very influential paper.

References

 

Aqueel, M. A., & Leather, S. R. (2012) Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids. Annals of Applied Biology, 160, 6-15.

Bakker, K. (1963) Backgrounds of controversies about population theories and their terminologies. Zeitschrift fur Angewandte Entomologie, 53, 187-208.

Burnett, T. (1951) Effects of temperature and host density on the rate of increase of an insect parasite. American Naturalist, 85, 337-352.

Elton, C. (1949) Population interspersion: an essay on animal community patterns. Journal of Ecology, 37, 1-25.

Glen, R. (1954) Factors that affect insect abundance. Journal of Economic Entomology, 47, 398-405.

Holling, C. S. (1959) Some characteristics of simple types of predation and parasitism. Canadian Entomologist, 91,385-398.

May, R. M. (1978) Host-parasitoid systems in patchy environments: A phenomenological model. Journal of Animal Ecology, 47, 833-844.

Solomon, M. E. (1969) Population Dynamics. Edward Arnold, London.

Southwick, C. H. (1955) The population dynamics of confined house mice supplied with unlimited food. Ecology, 36, 212-225.

Varley, G. C., Gradwell, G. R. & Hassell, M.P. (1973) Insect Population Ecology: An Analytical Approach. Blackwell Scientific Publications, Oxford.

Watt, K. E. F. (1959). A mathematical model for the effect of densities of attacked and attacking species on the numbers attacked. Canadian Entomologist, 91, 129-144.

 

Post script

A few months ago I was privileged to be given Robert Tillyard’s excellent The Insects of Australia and New Zealand (first published in 1926), by a former colleague of mine.

What made this even more special was that it had originally belonged to the great Maurice Solomon when he was a student, and contained some of his original annotations and revision notes.

 

Footnotes

*This is an expanded and updated version of the article I wrote as part of the British Ecological Society’s Centenary celebrations in 2013

**It is probably wishful thinking, but I might be tempted to think that by writing about this influential but somewhat overlooked paper, I increased the number of citations, so had a positive influence 🙂

***The Studies in Biology series, published by the then Institute of Biology (Now Royal Society of Biology), were excellent little books and the series on plant physiology were the main reason that I passed my first year plant physiology module as an undergraduate at Leeds University. I am reliably informed that there are plans to revive the series next year.

 

Entomological classics – The Tullgren (Berlese) Funnel

Although pitfall traps are great tools for getting an idea of what insects are running around on the soil surface or just below it, if you want to really understand the soil fauna you need to dig further down 🙂 There are a number of methods that you can use, sieving and flotation being very common (Southwood & Henderson, 2000). This is generally how entomologists sampled soil arthropods for many years (Greene 1880) despite the extra manual and time-consuming effort needed by the entomologist in addition to the initial digging. A more ‘natural’ and less time-consuming method is to let the arthropods do the work for you. Surprisingly, it was not until the beginning of the 20^th Century that an Italian entomologist, Antonio Berlese (1863-1927) came up with a more efficient and easy to use method. In essence he surrounded a 50 cm diameter metal funnel with a water jacket that could be heated,

Berlese funnel – direct heating version

either directly or indirectly using a Bunsen burner. The funnel was filled with soil or leaf litter and an alcohol filled tube placed at the base of the apparatus. The heat from the water jacket drives the insects and other arthropods down towards the collecting tube where they can be sorted at leisure. A much easier method than sieving and sorting. Berlese was very pleased with

Berlese funnel – indirect heating verison

his invention, and proudly comments “..consumes about three cubic meters of gas per day The above means that at a cost of about a lira I easily get in a day the same number of small animals that ten people with all the attendant discomfort and incredible patience would not be able to collect in the same time”* He points out that it is particularly good for collecting Collembola, Symphylids, Thysanurans and Pauropoda.

The first modification of the Berlese funnel was a minor one, that of Swedish entomologist, Ivar Trägårdh (1878-1951), with the water heated by spirit lamps instead of Bunsen burners, which meant that it was much more portable (Trägårdh, 1910).

First modification of the Berlese funnel, spirit lamps instead of Bunsen burners (Trägårdh, 1910).

The next modification was that of the German entomologist Anton Krausse (1878-1929). His design restricted the heated water jacket to the top part of the apparatus to drive the fauna downwards to the collecting tube and reduce the weight of the system. It was, however, still heated by a Bunsen burner.

The Krausse modification of the Berlese funnel (taken from Krausse, 1916).

A few years later, a Swedish arachnologist, Albert Tullgren (1874-1958) came up with a major modification, using an electric lamp to heat the surface of the soil or litter sample. The idea being that the drying effect was gradual and unidirectional and allowed the small insects and other invertebrates more time to find their way down to the collecting vessel before they died.

The Tullgren modification (Tullgren, 1917).

Tullgren points out that his apparatus is much cheaper to make and run. Interestingly, neither Berlese or Tullgren made any attempt to compare the efficiency of their methods for different components of the soil and litter fauna, presumably because they were just interested in collecting rather than comparing habitats. As far as I can tell the first person to compare and test different methods of using the funnels, e.g. having different strength of light bulbs and drying methods was Trägårdh (1933) who also compared different substrates with different initial water contents. Further work in the 1950s by the late, great, Amyan Macfadyen, additionally improved the reliability of the methods and interpretation of the data (MacFadyen, 1953, 1961). The Berlese or Berlese-Tullgren or Tullgren funnel, is now, and has been for over fifty years, an accepted part of the armoury of those studying the smaller members of the litter and soil, although there are a number of designs and descriptions.

From Smart (1949) Instructions for collectors (my Dad’s edition), here described as the Berlese funnel. The text also suggests that the heat can come from above e.g. a light source or even used outside with the sun ‘beating’ down on to the surface.

The illustration from Instructions for Collectors (my edition, (Cogan & Smith, 1973)) described in the text as Berlese funnel with Tullgren modification

Another example, this one from Southwood (1966) with no water jacket and a heating/drying unit at the top, with a light source at the bottom to attract(?) the soil fauna.

The Tullgren funnel array in use at Harper Adams University – light bulb for scale.

To use the above version you put your soil or litter sample in the upper part of the funnel which is removable, the lamp creates a temperature gradient, according to the manufacturers of approximately 14°C in the soil sample. To avoid the heating and drying effect, the soil arthropods, sieve themselves through the gauze to the collecting tube attached to the base of the funnel. In this version you can adjust the position of the lamp so that the drying process can be either slowed down or quickened up.

One of my PhD students, Fran Sconce (@FranciscaSconce) with her Tullgren funnels; the happy smile a testament to how much easier they are to use than manual sieving and flotation techniques 🙂

References

Berlese, A. (1905) Apparecchio per raccogliere persto en in gran numero piccoli artopodi. Redia, 2, 85-89.

Cogan, B.H. & Smith, K.G.V. (1973) Instructions for Collectors No 4a Insects, British Museums (Natural History) London

Greene, J. (1880) The Insect Hunter’s Companion: Being Instructions for Collecting and Describing Butterflies, Moths, Beetles, Bees, Flies, Etc.  

Krausse, A. (1916) Ein neuer automatischer Ausleseapparta besonder für terrikole Insekten un Milben. Zeitschrift für Angewandte Entomologie, 3, 303-304

Macfadyen, A. (1953) Notes on methods for the extraction of small soil arthropods. Journal of Animal Ecology, 22, 65-77.

Macfadyen, A. (1961) Improved funnel-type extractors for soil arthropods. Journal of Animal Ecology, 30, 171-184.

Smart, J. (1949) Instructions for Collectors, No 4A Insects, British Museum (Natural History), London.

Southwood, T.R. (1966) Ecological Methods, Chapman & Hall, London

Southwood, T.R.E. & Henderson, P.A. (2000) Ecological Methods, 3rd Edition, Blackwell Science, Oxford.

Trägårdh, I. (1910) Om Berlese’s apparat för snann och effecktiv insamling af små leddjur. Entomologisk Tiddskrift, 31, 35-37

Trägårdh, I. (1933) Methods of automatic collecting for studying the fauna of the soil. Bulletin of Entomological Research, 24, 203-214.

Tullgren, A. (1917) En enkel apprat för automatiskt vittjande av sällgods. Entomologisk Tidskrift. 38, 797-100

Post script

Modern Berlese funnels have totally morphed away from the original design and are much easier to use and deploy and store. You can also, very cheaply and easily make your own.

 http://www.nhbs.com/title/195607/standard-berlese-funnel-single?bkfno=211231&ca_id=1495&gclid=CK6qyrHgocwCFa0W0wodDcAJ7g

http://www.carolina.com/teacher-resources/Interactive/constructing-berlese-funnels-study-invertebrate-density-biodiversity/tr19101.tr

*a joint effort by me and Google Translate 

Ten Papers that shook my World – Root (1973) – When more means less – crop diversity reduces pest incidence

I can’t remember when I first read this paper but judging by the record card and the state of the actual hard copy of the paper, it was probably when I was doing my PhD in the late 1970s. This paper and its companion, which was published a year earlier* (Tahvanainen & Root, 1972), have had a significant effect on the scientific understanding and development of inter-cropping as a method of crop protection worldwide. Although inter-cropping in some form or another has been around a long time, the idea that it could be used as part of an integrated pest management programme was not proven.  In this landmark study, Root compared pure stands (plots) of collards (spring greens in the UK) (Brassica olercaea) with adjacent rows of collards grown intermingled with other herbaceous plants.  His premise being that it was well documented that pest outbreaks tend to be associated with pure monocultures of crops (Pimentel, 1961; Janzen, 1970) and he wished to test the hypothesis that natural enemies were more abundant and effective in vegetationally diverse areas  than in pure monocultures, the so-called ‘enemies hypothesis’.  This idea had been around a surprisingly long time e.g. Ullyett (1947) who remarked  “where weeds occur around headlands and in hedges, they should be left for the purpose of supporting parasites and predators important in the natural control of the diamond-back moth (Plutclla maculipennis Curt)”.  A decade later, Elton (1958,) refers to this statement, explaining that “these hedge rows form a reservoir for enemies and parasites of insects and mite pests of crops”.  I am not sure what it indicates but note that many groups around the world, including mine, are still working on this both at the local (field-scale) level (e.g. Ramsden et al., 2014) and landscape level (e.g. Rusch et al., 2013; Raymond et al., 2015).

Root explained the premise of the ‘enemies hypothesis’ as follows.  Predators and parasites are more effective at controlling herbivore populations in diverse habitats or plant communities because, diverse plant communities support a diversity of herbivores with a variety of phenologies, providing a steady supply of prey for the predators.  In addition, complex environments provide prey refugia, thus allowing the prey not to be completely eradicated.  Diverse plant communities also provide a broad range of additional resources for adult natural enemies e.g. pollen and nectar.

Root ran his experiment for three years and did indeed find a significant difference in herbivore load between the pure plots and the weedy rows, the former having a greater abundance of pests (mainly aphids and flea beetles) than the latter.

From Root (1973)

To his disappointment (I assume), he did not find any difference in the numbers of natural enemies between the two treatments. He thus had to come up with another idea to explain his results. His ingenious explanation is encapsulated in what he termed the Resource concentration hypothesis which states that herbivores are more likely to find and stay on hosts growing in dense or nearly pure stands and that the most specialised species often reach higher relative densities in simple environments.

Typical modern monocultures, beans, cabbages and wheat

He hypothesised that specialist herbivores were ‘trapped’ on the crop and accumulated whilst more generalist herbivores were able to and likely to move away from the crops to other host plants.  Root added that the ‘trapping effect’ of host patches depends on several factors such as stand size and purity.

In 1968, presumably as a result of what Root was discovering, Jorma Tahvanainen (one of the many great Finnish entomologists who appeared on the scene in the 1970s -, he retired in 2004) came to Cornell to do his PhD with Richard Root. Working on the same system and in the same meadow, Tahbanainen developed two new hypotheses to explain why more diverse cropping systems have fewer pest problems than monocultures. His experiments as he too found little evidence of natural enemies having an effect. He developed two new hypotheses, one he termed Associational resistance which I reproduce below exactly as published:

A natural community, such as a meadow, can be treated as a compound system composed of smaller, component communities (Root, 1973). The arthropods associated with different plant species represent important components in terrestrial systems. The available information indicates that the biotic, structural and microclimatic complexity of natural vegetation greatly ameliorates the herbivore pressure on these individual components, and consequently, on the system as a whole. Thus, it can be said that in a compound community there exists an “associational resistance” to herbivores in addition to the resistance of individual plant species. If the complex pattern of natural vegetation is broken down by growing plants in monocultures, most of this associational resistance is lost. As a result, specialized herbivores which are adapted to overcome the resistance of a particular plant species, and against which the associational resistance is most effective, can easily exploit the simplified system. Population outbreaks of such herbivores are thus more likely to occur in monocultures where their essential resources are highly concentrated

The other, is the Chemical Interference Hypothesis, in which he postulated that reduced herbivory in diverse communities due to chemical stimuli produced by non-host plants interfering with host finding or feeding behaviour of specialist herbivores.  His experimental set-up was very simple, but very effective.

How to send mixed signals to specialist herbivores – reproduced from Tahvanainen & Root (1972)

In simple terms, a monoculture sends out a very strong signal, it could be olfactory, e.g. a strong bouquet of crucifer volatiles, or for other herbivores it could be visual, or a combination of the two.

Conventional intensive agricultural landscape sending out strong ‘signals’ to specialist herbivores

Inter-cropping increases crop diversity and changes the crop ‘signal’ to one that now ‘confuses’ specialists. Note that I am not necessarily advocating a combined crop of wheat, beans and cabbages, as harvesting would be a nightmare 😉

 

The intercrop melange effect

These two papers have had a huge influence on the theory and practice of inter-cropping and agricultural diversification, although Root (1973) has had many more citations (1393 according to Web of Science on 11^th December 2015) than Tahvanainen & Root (1972) which has only had a meagre 429 citation to date.  The message coming out from the many studies that have now investigated the effect of intercropping crop diversification on pest abundance, is, that in general, polyculture is beneficial in terms of promoting biological control and that incorporating legumes into the system gives the best yield outcomes (Iverson et al,  2014).

Another take on intercropping that overcomes the potential problems of harvesting different crops from the same field, is the concept of planting different genotypes of the same species. Resistant plants tend to have fewer generalists present, although their individual yield may be reduced.  By planting a mixture of susceptible and resistant genotypes it is however, possible to have your cake and eat it, especially if it is not essential to have a single genotype crop.  This approach has been used to good effect in the production of short rotation willow coppice, where planting diverse genotypes of the same species reduces both pest and disease levels (Peacock et al., 2000, 2001).

Who would have that two simple field experiments conducted in an abandoned hay meadow outside Ithaca, New York almost fifty years ago would have such a far-reaching influence?

 

References

Elton, C. S. (1958) The Ecology of Invasions by Animals and Plants. London: Methuen & Co., Ltd. 159 pp.

Iverson, A. L., Makin, L. E., Ennis, K. K., Gonthier, D. J., Connor-Barrie, B. T., Remfret, J. L., Cardinale, B. J. &Perfecto, I. (2014). Do polycultures promote win-win or trade-offs in agricultural ecosystem services? A meta-analysis. Journal of Applied Ecology. 51, 1593-1602.

Peacock, L. & Herrick, S. (2000) Responses of the willow beetle Phratora vulgatissima to genetically and spatially diverse Salix spp. plantations. Journal of Applied Ecology, 37, 821-831.

Peacock, L., Hunter, T., Turner, H., & Brain, P. (2001) Does host genotype diversity affect the distribution of insect and disease in willow cropping systems? Journal of Applied Ecology, 38, 1070-1081

Janzen, D.H. (1970) The unexploited tropics.  Bulletin of the Ecological Society of America, 51, 4-7

Pimentel, D. (1961). Species diversity and insect population outbreaks. Annals of the Entomological Society of America, 54, 76-86.

Ramsden, M. W., Menéndez, R., Leather, S. R. & Wackers, F. (2014). Optimizing field margins for biocontrol services: the relative roles of aphid abundance, annual floral resource, and overwinter habitat in enhancing aphid natural enemies. Agriculture Ecosystems and Environment, 199, 94-104.

Raymond, L., Ortiz-Martinez, S. A. &Lavandero, B. (2015). Temporal variability of aphid biological control in contrasting landscape contexts. Biological Control , 90, 148-156.

Root, R. B. (1973). Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards. Ecological Monographs, 43, 95-124.  1393 citations

Rusch, A., Bommarco, R., Jonsson, M., Smith, H. G. &Ekbom, B. (2013). Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. Journal of Applied Ecology, 50, 345-354.

Tahvanainen, J. & Root, R. B. (1972). The influence of vegetational diversity on the population ecology of a specialized herbivore Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia, 10, 321-346. 429 citations

Ullyett, G. C. (1947) Mortality factors in populations of Plutella maculipennis Curtis (Tineidae: Lep.) and their relation to the problem of control. Union of South Africa, Department of Agriculture and Forestry, Entomology Memoirs, 2, 77-202.

Post script

*I suspect, judging by how the two papers cite each other, that the Root (1973) paper was actually submitted first but that the vagaries of the publication system ,  meant that follow-up paper, Tahvanainen & Root (1972) appeared first.

Entomological classics – the Window (pane) Flight Intercept Trap

A couple of years ago I received a paper to review in which the authors detailed how they had invented a new trap for sampling and collecting beetles in tropical forests. I was astounded to see that they were describing a window pane trap, something that I had known about since I was a student and which has been used by entomologists worldwide for many years.  I quite politely pointed this out in my review and directed the authors to Southwood ‘s Ecological Methods (1966).  The other referee was less tolerant, her/his report simply read “see Southwood page 193”.  At the time I wrote the review it was firmly stuck in my mind that the technique was as old as the hills, or at least as old the invention of cucumber frames 🙂  I certainly thought of it as a Victorian or Edwardian invention.  To my surprise when I started delving into the literature all the Victorian references to window traps turned out to be ways to protect households from invasion from houseflies and other unwanted flying insects; nothing to do with entomological sampling or collecting. E.g. this patent from 1856 where the inventor describes its operation as follows “The flies enter the trap through the passage B, as illustrated, and after satisfying their wants from the baitboard seek to escape, and being attracted by strong light from the glass back they fly in that direction and being headed out crawl up the glass back until they nearly reach the upper edge of the same, when, being still attracted and deluded by light from the glass top, they attempt to fly upward or through the same and in doing so instead of rising, are, owing to the inclination of the glass top, precipitated into the trough of soap suds and drowned, as illustrated in the drawing.

This fly trap is exceedingly simple, quite cheap, and only costs about twenty-five cents, and has been tried and found to answer well the purpose intended.”

Unfortunately not what I was looking for 🙂

Despite scouring Google and Google Scholar, to the lengths of even getting to page 30, which apparently no-one does, it seems that the earliest reference to what we think of as a Window (pane) trap was not invented until 1954 (Chapman & Kinghorn, 1955)  to sample Ambrosia beetles (Trypodendron spp.) and other scolytids in Canadian forests.  There is unfortunately no picture to illustrate the trap, but the written description is fairly clear “ a piece of window glass (2 X 2 ft) set in a three-sided wooden frame from which a sheet metal trough is hung. The trough is filled with fuel oil or water….Traps are hung from various types of pole framework  depending on their location, and guy wires are used to keep them from swinging.”  I am pretty certain that this 1954 date is the earliest record as even that vade mecum of the entomologist, Instructions for Collectors No. 4a (Smart, 1949) has no mention of it.

The theory behind the window (pane) trap is that flying insects are unable to see the clear glass (or Perspex), bang into it, and stunned, fall into the collecting trough where they drown to be collected and identified later. A fantastically simple idea, which is why I was surprised that it took entomologists so long to invent it. As far as I can tell from the written description given by Chapman & Kinghorn (1955), the trap was suspended from a ground based framework.  I think that this version I found in Chapman (1962) is probably the original design or at least very close to it.

Chapman & Kinghorn’s original window flight trap? Chapman (1962).

They also used this is a much more ambitious way as shown below.

Multiple Chapman & Kinghorn Window traps in operation (Chapman & Kinghorn, 1958).

This design in a slightly modified version  is shown in Lundberg (1979) and designs very

Ground based window trap in use in a Swedish forest (Lundberg, 1979).

similar to these are still in use.

A modern ground-based window(pane) flight intercept trap. http://www.qm.qld.gov.au/Find+out+about/Animals+of+Queensland/Insects/Collecting+insects/~/media/51C96B0159AF463C9E11CC1B100244DE.jpg?w=400&h=260&as=1

 

Despite its efficiency the ‘classic’ windowpane trap has perhaps not been used as much as it deserves, instead, a plethora of alternative designs have been described since the mid-1970s. So for example we have a small-scale tree hanging version, with a four-way window being used to catch forest coleoptera (Hines & Heikkenen, 1977).  Although the small area flight intercept traps were

 

The Hines & Heikkenen (1977) small area window flight intercept trap.

relatively easy to deploy, they obviously just weren’t big enough for some people. In 1980, Peck & Davies, described a large-area window trap used to catch small beetles. This used the central panel of a Malaise trap as the window under which they placed a large metal collecting trough.  Unlike the Hines & Heikkenen trap, this like the original Chapman & Kinghorn trap, was ground-based.  The

The Peck & Davies(1980) large-area “window” trap.

authors, in an attempt to impose order on to the entomological collecting world, urge other coleopterists to adopt a similar trap design.  In 1981 we see a modification to the Hines & Heikkenen

The Omnidirectional flight trap (Wilkening et al., 1981).

trap to improve its efficiency (Wilkening et al., 1981).  Despite the name omnidirectional, implying that it catches insects from all directions,  this trap catches large fast-flying insects in the lower chamber, into which they fall stunned on bumping into the window pane and slow upwards flying insects in the upper chamber.  The authors argue that the original version of the trap did not catch slow-flying insects as they were able to detect the pane early enough to avoid being stunned and then took evasive action by flying up and away from the collecting bottle.  The new improved version takes advantage of this behaviour and traps them in the upper bottle into which they inadvertently fly.

In 1988, my fellow editor, Yves Basset, then at Griffiths University in Australia, now at the Smithsonian Tropical Research Institute in Panama, decided to combine a Malaise trap with a Hines & Heikkenen trap to produce what he called a composite interception trap (Basset, 1988),

The Basset composite interception trap (Basset, 1988).

The Basset composite trap in action. http://web.uvic.ca/~canopy/sampling.html

 

Despite this ingenious trap, trapping forest canopy insects obviously continued to occupy the minds of forest entomologists and in 1997 another pair of entomologists working in Australia came up with yet another design for a flight intercept trap, this time one that could be suspended at different heights in the canopy and left for long periods of time (Hill & Cermak, 1997). The novelty of this trap

The Hill & Cermak modified Window trap

 

as far as I can make out is the use of multiple collecting chambers (ice cream tubs) and a plastic instead of a Perspex, ‘window’.

Entomologists are forever tinkering and ‘improving’ with sampling methods, so it should not be a surprise to find a group of entomologsist from the USA describing the ultimate in a composite trap,  this time a combination of four different traps, the cone, the Malaise, the yellow pan trap and the flight intercept trap (Russo et al., 2011). Interestingly, the authors describe this as a passive trap,

The ultimate composite insect trap (Russo et al., 2011).

but as it incorporates a yellow pan trap, which actively attracts insects, this is not strictly true.

Returning to the more conventional flight intercept trap design, Lamarre et al (2012) compared their very slightly modified window pane trap with Malaise traps in tropical forests in French Guiana and

According to the paper, the first attempt to develop a standardised Window pane trap. https://commons.wikimedia.org/wiki/File%3AA_modified_windowpane_trap.jpeg

concluded that their model was more efficient and “should be used as an alternative and standardised method for future empirical studies”  a bold statement indeed, as they did not compare their trap with any of the other traditionally used window pane traps described above.

And finally and right up to date, and in the best entomological tradition of using cheap easily obtainable materials, yet another variant on the flight intercept trap; this time using plastic bottles – pop, soda, water, cider, beer, take your pick J (Steininger et al., 2015).

The simple, effective and accessible bottle window intercept trap. http://jee.oxfordjournals.org/content/108/3/1115

I am sure, however, that as I write, some ingenious entomologist out in the field somewhere, is thinking of yet another modification to the window (pane) flight intercept trap to make my post out of date!

 

References

Basset, Y. (1988) A composite interception trap for sampling arthropods in tree canopies.  Journal of the Australian Entomological Society, 27, 213-219

Chapman, J.A. (1962) Field studies on attack flight and log selection by the ambrosia beetle Trypodendron lineatum (Oliv.) (Coleoptera: Scolytidae). Canadian Entomologist, 94, 74-92

Chapman, J.A. & Kinghorn, J.M. (1955) Window flight traps for insects.  Canadian Entomologist, 87, 46-47.

Chapman, J.A. & Kinghorn, J.M. (1958) Studies of flight and attack activity of the ambrosia beetle, Trypodendron lineatum (Oliv.) and other Scolytids. Canadian Entomologist, 90, 362-372

Hill, C.J. & Cermak, M. (1997) A new design and some preliminary results for a flight intercept trap to sample forest canopy arthropods.  Australian Journal of Entomology, 36, 51-55

Hines, J.W. & Heikkenen, H.J. (1977) Beetles attracted to severed Virgina pine (Pinus virginiana Mill.). Environmental Entomology, 6, 123-127

Lamarre, G.P.A., Molto, Q., Fine, P.V.A. & Baraloto, C. (2012) A comparison of two common flight interception traps to survey tropical arthropods.  ZooKeys, 216, 43-55

Lundberg, S. (1979) Fångst av skallbaggar med hjälp av fönsterfällor. Entomologisk Tidskrift (Stockolm), 100, 29-32

Peck, S.B. & Davies, A.E. (1980) Collecting small beetles with large-area “window” traps.  Coleopterists Bulletin, 34, 237-239

Russo, L., Stehouwer, R., Heberling, J.M. & Shea, K. (2011) The composite insectrrap: an innovative combination trap for biologically diverse sampling.  PLoS ONE, 6, e21079.doi:10.1371/journal.pone.0021079

Wilkening, A.J., Foltz, J.L., Atkinson, T.H. & Connor, M.D. (1981) An omnidirectional flight trap for ascending and descending insects.  Canadian Entomologist, 113, 453-455

 

Postscript

Apropos of the ultimate composite trap, I came across this combination four-way window-yellow pan trap combination some years ago, but have not been able to find a published inventor of it.  I should also add that flight intercept traps are also sometimes known as impact traps.

*Vade mecum, a handbook or guide that is kept constantly at hand for consultation.

 

Entomological classics – the Light Trap

I think that even those of us who are not entomologists are familiar with the attraction that insects, particularly moths, have for light. The great Sufi philosopher Bahauddin Valad (1152-1231) wrote the following lines

a candle has been lit

inside me,

for which

the sun

is a moth.

 

In Shakespeare’s The Merchant of Venice (1596), Portia famously declaims “Thus hath the candle singed the moath.”

It may thus come as a bit of surprise to realise that ‘modern’ entomologists were quite slow to develop bespoke traps that took advantage of this aspect of insect behaviour. That said, according to Beavis (1995) the Roman author Columella (Lucius Junius Moderatus, 4-7 AD), describes a light trap to be used to protect bee hives from wax moth attacks. A pretty much identical trap was still being used in 1565 (Gardiner, 1995) although he erroneously calls it the first light-trap. As far as I can tell the early ‘modern’ Lepidopterists used the white sheet technique, still used today, where a light source such as a paraffin lamp (nowadays an electric light or powerful torch) was suspended above or behind a white sheet, from which the intrepid entomologist collected specimens of interest that come to rest on the sheet. This can be very efficient but does require the entomologist to be ‘on duty’ throughout the trapping

The white sheet technique.

period, although on a fine night, with good companionship and an ample supply of beer, or other alcoholic beverage, it can be a very pleasant way to spend a long evening 😉

The earliest published reference to a modern bespoke light trap that I have been able to find is a patent from 1847 for a modified beehive which includes a light trap to lure wax moths away from the main part of the hive (Oliver Reynolds, 184, US Patent5211; http://www.google.com/patents/US5211).

The modified Reynolds Beehive incorporating moth trap.

The second published reference to a bespoke light trap is again one designed to control wax moths and is described in a patent application by J M Heard dated 1860. In this case as far as I can make out the lamp is actually glass coated with a phosphorescent material rather than using a candle or oil flame.

“The basin A, is supplied with a requisite quantity of molasses or other suitable substance to serve as a bait, and the inner sides of the glass plates c, of the lamp C, are covered with a mixture of phosphorus and oil or phosphorus combined with any suitable substance to form a cement, or a stick E, may be coated with the cement, said stick being passed through the tube e, into the lamp, as shown plainly in Fig. 1. The insects decoyed by the light and attracted by the bait, strike against the inclined glass plates c, and fall into the basin A. By having the plates c, inclined the insects are made to fall through the opening b, into the basin and said opening is permitted to be comparatively small and the cover a, of the basin in connection with the cover D, of lamp protect perfectly the bait from sun and rain, thereby protecting an unnecessary waste of the same. During the day the phosphorus of course is not needed unless it be cloudy, but the device is chiefly efficacious at night as the visits of the insects are mostly nocturnal.”

So whilst beekeepers and agriculturalists were busy using traps to attract moths to kill them what were the lepidopterists doing? It appears that they were using whole rooms as light traps as described here by H T Stainton in 1848.

 

A later Victorian entomological ‘how to’ book, added instructions of how to use gas and paraffin lamps outside, with the lepidopterist standing ready with his net (Greene, 1880).

The 20^th Century was however, when we see the birth of the light traps as we know them today. First on the scene was the Rothamsted Trap, developed by the great C B Williams, which was

 

The electric ‘fixed’ Rothamsted Trap.

The ‘portable’ Rothamsted Trap – Williams (1948)

developed from earlier versions that he used in the 1920s and 1930s, in Egypt and England (Williams, 1924, 1935).

Rothamsted trap in action

 

Apparently the first electrical light trap to use an ultra-violet light was made in 1938 (Barratt, 1989) and used in the 1940s (Fry & Waring, 2001) but it was not until 1950 that the first commercially available version was produced (Robinson & Robinson, 1950).

The Robinson Trap – very popular and ideal for use in gardens where there is easy access to a mains supply.

 

Strangely, considering that the Americans had been first on the scene with patented light traps it was not until 1957 that the Pennsylvanian and Texas traps appeared on the scene (Frost, 1957) closely followed by the Texas traps (Hollingsworth et al., 1963). These traps used fluorescent tubes instead of bulbs and were particularly good at catching beetles, moths and ants. The Texas trap and the Pennsylvania trap were essentially the same, the main difference being that the Pennsylvania trap has a circular roof to prevent train entering the killing bottle. As Southwood (1966) somewhat tongue in cheek says, this may reflect the differences in the climate of the two states 😉

The Pennsylvanian Light Trap.

In the 1960s the Heath Trap appeared on the scene (Heath, 1965). This was billed as being extremely portable, being able to be carried in a back pack and also able to be run either from a mains supply or from a 12 volt battery.

The Heath Light trap.

Less expensive and more portable is the Skinner trap, (designed by Bernard Skinner in as far as I can make out in the early 1980s, please let me know if you know exactly) which comes in wooden and aluminium versions and is collapsible, so that if needed, several can be transported at once. It comes in both mains and battery versions.

  

The Skinner light trap – relatively inexpensive and very portable.

An interesting combination of light and odour being used to attract and trap insects, in this case to ‘control’ them, is the Strube Stink bug trap. This is an American invention and is used to protect US householders against the the Brown Marmorated Stink Bug, Halyomorpha halys, an invasive species from Asia which appears to have developed a propensity to overwinter in people’s houses. I remember a few years ago that we in the UK were warned that it might cross the channel from France; this resulted in lurid headlines in the ‘Red Top’ newspapers with wording like ‘stench spraying insect’ being used 😉

Strube Stink Bug Trap

 

This appears to be a very effective trap; all the reviews I have read praise it highly, so if the Brown Marmorated Stink Bug does make it to the UK, the Strube trap will be the one to buy!

 

References

Frost, S.W. (1957) The Pennsylvanian light trap. Journal of Economic Entomology, 50, 287-292.

Fry, R. & Waring, P. (2001) A Guide to Moth Traps and their Use. Amateur Entomologist, Orpington, Kent.

Gardiner, B.O.C. (1995) The very first light-trap, 1565? Entomologist’s Record and Journal of Variation, 107, 45-46

Greene, J. (1880) The Insect Hunter’s Companion. W. Swan Sonnenschein & Allen, London.

Heath, J. (1965) A genuinely portable MV light trap. Entomologist’s Record and Journal of Variation, 77, 236-238.

Hollingsworth, J.P., Hartstock, J.G. & Stanley, J.M. (1963) Electrical insect traps for survey purposes. U.S.D.A. Agricultural Research Service 42-3-1, 10 pp.

Robinson, H.S. & Robinson, P.J.M. (1950) Some notes on the observed behaviour of Lepidoptera in the vicinity of light sources together with a description of a light trap designed to take entomological samples. Entomologist’s Gazette, 1, 3-20

Southwood, T.R.E. (1966) Ecological Methods. Chapman & Hall, London

Stainton, H.T. (1848) On the method of attracting Lepidoptera by light. The Zoologist, 6, 2030-2031

Williams, C.B. (1924) An improved light trap for insects. Bulletin of Entomological Research, 15, 57-60.

Williams, C.B. (1935) The times of activity of certain nocturnal insects, chiefly Lepidoptera, as indicate by a light-trap. Transactions of the Royal Entomological Society of London B, 83, 523-555.

Williams, C.B. (1948) The Rothamsted light trap.   Proceedings of the Royal Entomological Society of London A, 23, 80-85.

 

Post script

There are of course more light traps out there, many being variations of those described above, or for specific insect groups such as mosquitoes or aquatic traps for Cladocera (water fleas). Many ‘home made’ traps also exist, such as the ‘portable’ one I made for use on the field course that I used to run at Silwood Park.

The Leather Light Trap

I used a rechargeable battery lantern, but other light sources would also work. In retrospect I should have painted the Perspex black so that only the ‘entrance’ funnels emitted light. There was a tendency for insects to sit on the outside of the trap rather than enter it.

A useful link for those wishing to make their own traps can be found here http://www.theskepticalmoth.com/techniques/light-traps/ and Fry & Waring (2001) also has some very useful hints and tips.

 

 

Ten Papers that Shook My World – Haukioja & Niemelä (1976) – the plant “immune response”

To me this is a landmark paper, both personally and for ecology in general.   I first came across it in the second year of my PhD at the University of East Anglia (1978) and given where it was published, would probably never have seen it if my supervisor, Tony Dixon, hadn’t had a collaborative link with Erkki Haukioja of Turku University (Finland).

That individual plants of the same species are more or less susceptible (constitutive or innate resistance) to pests and diseases has been known for a very long time (e.g. Painter, 1958; Beck, 1965) and has been exploited by plant breeders as part of many pest management programmes.  Despite the stunning footage of the questing bramble in David Attenborough’s classic documentary The Private Life of Plants, plants are often thought of as passive organisms.  The idea that plants might actually respond directly and quickly to insect attack was more in the realms of science fiction than science fact, but this all changed in the 1970s. In 1972 a short paper in Science (Green & Ryan, 1972) suggested that plants might not be as passive as previously thought. Green & Ryan working in the laboratory with the Colorado Potato Beetle, Leptinotarsus decemlineata, showed that when tomato leaves were damaged by beetle feeding the levels of a proteinase inhibitor were raised not just in the wounded leaves but in nearby leaves as well. As proteinase inhibitors were well-known to be part of the plant defence system, they hypothesised that this was a direct response of the plant to repel attack by pests and that it might be a useful tool in developing new pest management approaches. So what does this have to do with two Finnish entomologists?

Erkki Haukioja and his long-term collaborator, Pekka Niemelä were working on an important lepidopteran defoliator of birch, in the far north of Finland, at the Kevo Subarctic Research Station.

http://www.eu-interact.org/field-sites/finland-4/kevo/

The defoliator that they were working on was the autumnal moth, now Epirrita autumnata, but then Oporinia autumnata.

http://ukmoths.org.uk/show.php?bf=1797

The autumnal moth, as with many tree-feeding Lepidoptera, has a 7-10 year population cycle (Ruohmäki et al., 2000).

Natural enemies are often cited as the causes of these cycles (Turchin et al., 1999) although other factors such as weather (Myers, 1998) or even sunspot activity (Ruohmäki et al., 2000)

have also been suggested. It had also been suggested that the marked population cycles of the larch bud moth, Zeiraphere diniana were caused by changes in the susceptibility of their host trees after defoliation (Benz, 1974). In 1975, Haukioja and his colleague Hakala, attempting to explain the cyclical nature of the E. autumnata population cycles wondered if they were being driven by the insects themselves causing changes in the levels of chemical defence in the trees. To test this Erkki and Pekka did two neat field experiments, remember Green & Ryan’s work was laboratory based and did not test the effects seen on the insects. They first fed Epirrita larvae on foliage from previously defoliated and undefoliated birch trees and found that the pupae that developed from those larvae fed on previously defoliated trees were lighter than those that had fed on previously undefoliated trees (Hauikioja & Niemelä, 1976). At the same time they also did an experiment where they damaged leaves but then rather than feeding the larvae on those leaves, fed them on nearby adjacent undamaged leaves and compared them with larvae feeding on leaves from trees where no damage had occurred. Those larvae feeding on undamaged leaves adjacent to damaged leaves grew significantly more slowly than those feeding on leaves that came from totally undamaged trees (Haukioja & Niemelä, 1977). So pretty convincing evidence that the trees were responding directly to insect damage and altering their chemistry to become more resistant, i.e. an induced defence and not a constitutive one.

Their results had a major impact on the field. The great and the good from around the world found it a fascinating subject area and a plethora of papers investigating the effects of insect feeding on induced defences in birch and willow trees soon followed (e.g. Fowler & Lawton, 1984a; Rhoades, 1985; Hartley & Lawton, 1987) and not forgetting the original researchers (e.g. Haukioja & Hahnimäki, 1984). I, with the aid of colleagues, also added my ‘two pennorth’ (I did say the idea shook my world) by extending the concept to conifers (Leather et al., 1987; Trewhella et al., 1997). The terms rapid induced resistance and delayed induced resistance soon entered the language, the first to describe those changes that occurred within minutes of feeding damage and the second, those that did not take effect until the following year (Haukioja & Hahnmäki, 1984; Ruohmäki et al., 1992) Such was the interest generated by the topic that by 1989 there were enough studies for a major review to be published (Karban & Myers, 1989).

Controversy reared its ugly head early on when Doug Rhoades suggested that not only did plants resist insect attack actively but that they could talk to each other and warn their neighbours that the ‘bad guys’ were in the neighbourhood (Rhoades, 1983, 1985). This sparked a brief but lively debate (e.g. Fowler & Lawton, 1984b, 1985). Ironically it is now taken as axiomatic that plants talk to each other using a range of chemical signals (van Hulten et al., 2006; Heil & Ton, 2008) as well as informing the natural enemies of the pests that a suitable food source is available (e.g. Edwards & Wratten, 1983; Amo et al., 2013; Michereff et al., 2013).

A great cartoon from Jurriaan Ton at Sheffield University. https://www.shef.ac.uk/aps/staff-and-students/acadstaff/ton-jurriaan

We now have a greatly increased understanding of the various metabolic pathways that induce these defences against different insect pests (e.g. Smith & Boyko, 2007) and can, by genetically manipulating levels of compounds such as jasmonic and salicyclic acids or even applying them directly to plants affect herbivorous insect communities and their natural enemies thus improving crop protection (e.g. Thaler, 1999; Cao et al., 2014; Mäntyllä, 2014). No wonder this was an idea that shook my world, and yours.

 

Post script

The study of induced plant defences or resistance is now dominated by molecular biologists and current practice is to use the term priming and not induced defence. The increased understanding that this new generation has brought to the field is undeniable but I always feel it is a great shame that they seem to have forgotten those early pioneers in the field.

 

References

Amo, L., Jansen, J.J., Van Dam, N.M., Dicke, M., & Visser, M.E. (2013) Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecology Letters, 16: 1348-1355.

Baldwin, I.T. & Schultz, J.C. (1983) Rapid changes in tree leaf chemistry, induced by damage: evidence for communication between plants. Science, 221, 277-279.

Beck, S.D. (1965) Resistance of plants to insects. Annual Review of Entomology, 10, 207-232.

Benz, G. (1974). Negative Ruckkoppelung durch Raum-und Nahrungskonkurrenz sowie zyklische Veranderung. Zeitschrift für Angewandte Enomologie, 76: 196-228.

Cao, H.H., Wang, S.H., & Liu, T.X. (2014) Jasomante- and salicylate-induced defenses in wheat affect host preference and probing behavior but not performance of the grain aphid, Sitobion avenae. Insect Science, 21, 47-55.

Edwards, P.J. & Wratten, S.D. (1983) Wound induced defences in plants and their consequences for patterns of insect grazing. Oecologia, 59: 88-93.

Fowler, S.V. & Lawton, J.H. (1984a) Foliage preferences of birch herbivores: a field manipulation experiment. Oikos, 42: 239-248.

Fowler, S.V. & Lawton, J.H. (1984b) Trees don’t talk : do they even murmur? Antenna, 8: 69-71.

Fowler, S.V. & Lawton, J.H. (1985) Rapidly induced defences and talking trees: the devils’ advocate position. American Naturalist, 126: 181-195.

Green, T.R. & Ryan, C.A. (1972) Wound induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science: 175: 776-777.

Hartley, S.E. & Lawton, J.H. (1987) Effects of different types of damage on the chemistry of birch foliage and the responses of birch feeding insects. Oecologia, 74: 432-437.

Haukioja, E. & Hakala, T. (1975) Herbivore cycles and periodic outbreaks. Report of the Kevo Subarctic Research Station, 12: 1-9

Haukioja, E. & Hanhimäki, S. (1984) Rapid wound induced resistance in white birch (Betula pubescens) foliage to the geometrid Epirrita autumnata: a comparison of trees and moths within and outside the outbreak range of the moth. Oecologia, 65, 223-228.

Haukioja, E. & Niemelä, P. (1976). Does birch defend itself actively against herbivores? Report of the Kevo Subarctic Research Station 13: 44-47.

Haukioja, E. & Niemelä, P. (1977). Retarded growth of a geometrid larva after mechanical damage to leaves of its host tree. Annales Zoologici Fennici 14: 48-52.

Heil, M. & Ton, J. (2008) Long-distance signalling in plant defence. Trends in Plant Science, 13: 264-272.

Karban, R. & Myers, J.H. (1989) Induced plant responses to herbivory. Annual Review of Ecology & Systematics, 20: 331-348.

Leather, S.R., D., W.A., & Forrest, G.I. (1987) Insect-induced chemical changes in young lodgepole pine (Pinus contorta): the effect of previous defoliation on oviposition, growth and survival of the pine beauty moth, Panolis flammea. Ecological Entomology, 12: 275-281.

Mäntyllä, E., Blande, J.D., & Klemola, T. (2014) Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod-Plant Interactions, 8, 143-153.

Michereff, M.F.F., Borges, M., Laumann, R.A., Dinitz, I.R., & Blassioli-Moraes, M.C. (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telonomus podisi. Entomologia experimentalis et applicata, 147: 9-17.

Trewhella, K.E., Leather, S.R., & Day, K.R. (1997) Insect induced resistance in lodgepole pine: effects on two pine feeding insects. Journal of Applied Entomology, 121: 129-136.

Myers, J. H. (1998). Synchrony in outbreaks of forest lepidoptera: a possible example of the Moran effect. Ecology 79: 1111-1117.

Painter, R.H. (1958) Resistance of plants to insects. Annual Review of Entomology, 3: 267-290.

Rhoades, D.F. (1983) Responses of alder and willow to attack by tent caterpillar and webworms: evidence for pheromonal sensitivity of willows. American Chemical Society Symposium Series, 208: 55-68.

Rhoades, D.F. (1985) Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. American Naturalist, 125: 205-238.

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