Some fantastic sculptures but a sad lack of insects

A couple of weeks ago my wife and Daughter #2 and I, took advantage of the late Bank Holiday Weekend to visit The Sculpture Park near Farnham.  For a Bank Holiday weekend the weather was pretty good, the sun decided to shine 😊

As the name suggests the park is set in a wooded valley with ponds, streams and small lakes, all of which are used to good purpose, the sculptures, most of which are for sale*, placed in appropriate locations.

At £10 each it was pretty good value; on the day we visited there were 850 sculptures on site.  You could, if you were so minded, walk around for free, but the £10 gives you access to a guide to the sculptures, including their prices* and directions to navigate the site.  Without the guide, you could have an enjoyable walk, but you would certainly miss a lot.  There is also an on-site shop if you want to spend more money and help the enterprise prosper 😊

I took a lot of photos, concentrating mainly on the natural history based themes, not of all of which I am going to share, but hopefully those I do will give you an idea of the site.

The site starts some distance before you reach the ticket office.  The sculptures are in a variety of materials and styles, stone, metal, fibre-glass and wood, abstract, odd and realistic.

Is this what the toads were heading towards?

The site makes great use of the natural features and there are many surprises lurking in bushes, around corners and above your head.

 Continuing with the watery theme

Amazing what you find lurking in the trees 🙂

and don’t forget to look above head height.

Perhaps the birds closer to the ground should be wary of the polar bear?

Woodland scenes

Waste not, want not, especially if you can sell it as art 🙂

Some very odd stuff – Listening for the boneshaker?

More phantasmagorical beings

These woodland denizens however, you might be forgiven for thinking are real

Beautiful

Even as an entomologist I thought this was great – Rutting stags in wood

And there were some insects, a couple of mantids ready to pounce on the unsuspecting visitor

Metallic arthropods

Invertebrates were, however, in very short supply, so even snails made it into my selection 🙂

 

Some days I feel like this 🙂

 

The Aurelian – way out of my price range 🙂

And to finish – a three dimensional play on words

 

It was a great place to visit, despite the dearth of invertebrate exhibits. Most of the sculptures were based on humans, which I seem not to have photographed 🙂  That said we did only see 420 of the sculptures, perhaps there were more invertebrates in the remaining 440! I somehow doubt it.  Going by this it would seem that sculptors, like the majority of the public, are institutionally vertebratist ☹ That said, French sculptor Edouard Martinet makes larger than life insect sculptures using old car parts and his work would certainly fit in well here.

A word of warning, parking is at a premium. We had to park a good ten minutes walk away from the entrance.  There there is a picnic area, but alas, no café,  and as you will need to spend a minimum of four hours to get around all the sculptures, it is well worth making a day of it and taking ample supplies of food and drink.

*prices ranging from a few hundred pounds to tens of thousands  :-0

 

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Pick and mix 19 – a mixed bag

George Monbiot on how big coroporations are using viral marketing techniques to rubbish their opponents and even get scientific papesr retracted – very disturbing if true

When should a non-aggressive exotic species be demoted to a harmless naturalized resident?

David Zaruk on the two sides of communicating the perceived and real risks of pesticides

It turns out that moths and butterflies are a lot older than we thought – 70 000 000 years older!

More evidence that plants talk to each other

Why imaginary treehouses help children engage with Nature

Embedding real insects in resin – a great outreach tool

Taxonomy is essential for global conservation, not a hindrance

Why you shouldn’t kill or remove your house spiders

And yet more evidence to show that insects are under threat, this time from climate change

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Working from home in France

My wife and I are lucky enough to own a second home in France, in the Pays D’Oc. Hopefully, when we fully retire, it will be our main, if not only home.  At the moment, I get to spend much less time there than I would like, but since I semi-retired this academic year, the frequency of my visits has increased.

I have just finished a two-week spell there, not on holiday, but working from home, five days of which were spent working on a field skills handbook with two former colleagues of mine from Imperial College who used to help me run our two-week long final year Biodiversity & Conservation Field Course.  We have been working on this book for more than six years but to say that progress had been snail-like would be an exaggeration, glacial would be a better description.

Being away from our respective campuses, and the day-to-day academic trivia, meant that we were able to concentrate fully on the task at hand. We made incredible progress, and that was despite being connected to the internet and having access to Skype and email.  We now, in just five days and with very relaxed lunch-times, have a pretty good skeleton to show our prospective publisher.   A proper retreat works wonders; I can thoroughly recommend it.  It would be great if I could persuade my Head of Department to fund an official retreat for me and some of my colleagues to get together to write papers and grant proposals. It would definitely repay itself in increased grant income 🙂

The authors, looking relaxed but thinking hard.

The location certainly helps, with an office window view like this, who can help but be inspired 😊

The view from my office

 

In fact, I was so inspired I turned to verse.

 

Mountainous thunder

Sends ants scuttling to their nest.

Seeds await the wind

#haiku

 

Ants, sensing distant thunder,

Scuttle to their nest,

While seeds pods wait for the wind

#reversehaiku

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Waifs and strays – those papers nobody cites (or reads?)

I guess, like most, if not all of us, who publish papers, we hope that not only will our papers be read, but that they will be cited by others, not just ourselves.  From a purely practical point, it is after all, how academics impress promotion boards or prospective employers. From a more personal point of view, the papers we publish represent a lot of effort, not just in gathering the data or having the idea, but also the nightmare of turning it into deathless prose and then the battle with editors and reviewers.  We all have a few papers that we hope will make our name and perhaps become a citation classic, although as Stephen Heard has pointed out not just once, but twice, our favourites are not always everyone else’s, with some papers significantly failing to meet expectations.  A recent article in Times Higher Education, showed that in some disciplines, notably in the arts, 77% of papers were still uncited five years after publication and even in the sciences, about 40% of papers suffered a similar fate.  For ecologists, the hot area is ecological modelling, with only 6% of papers remaining uncited after five years. As someone with an advanced case of imposter syndrome, this is really quite reassuring; although I have twelve papers that are uncited (according to Web of Science), they only represent 6% of my output (and I am not a modeller 😊), of which only one dates back to 2012 (0.5%).  I do, however, have another 34 papers, that although they have been cited, have been cited fewer than five times, 17% of my output, or, if I add in my never been cited papers, 23% of my work has had relatively little impact on the ecological and entomological world.

Despite this, I was curious about what, if anything, these unwanted (=uncited) waifs and strays had in common, and how they differed from my most cited papers; absolutely nothing to with the fact that Stephen Heard only had four zero papers, all of which were recent papers 😊 In Steve’s analysis he looked at time since publication and found a positive correlation, his oldest papers had accrued the most citations.  I have a somewhat larger corpus of work than Steve, so concentrated my analysis on my top twenty papers.  There was absolutely no relationship (Figure 1), all pretty much of a muchness apart from the massive outlier, but even with that removed, still nada.

Figure 1. My top twenty papers.  The massive outlier is my single Annual Review of Entomology paper.

My least cited papers, do however, show a relationship between years since publication and the paltry number of citations that they have received (Figure 2).

Figure 2. The foot of the table papers.

If I combine the two data sets and leave out my star paper, there is a relationship between time since publication and the number of citations gained (Figure 3), so I expect, but I could be wrong, and I am not going to invest the time in finding out, that if I analysed all my papers that there would be a similar relationship as that shown by Steve’s analysis.

Figure 3. Relationship between time since publication and number of citations accrued for my most and least cited papers (excluding the massive outlier).

So, what makes a paper a waif, or reversing the question, a star?  Editors, of which I am one, are great fans of Reviews, believing, usually correctly, that they garner a lot of Impact Factor points, authors perhaps less so, as they tend to take away citations from your other papers. After all, who writes a review without citing themselves? 😊 The other thing that helps a paper get cited is their title, Andrew Hendry over on Eco-Evo Evo-Eco suggests that two main factors come into play. The first is that those papers that have a very good “fill in the box” titles are much more likely to be cited than those with more specific titles. He points out that a paper he and colleagues published in Philosophical Transactions of the Royal Society of Biology paper is the only one in the literature with Eco-Evolutionary Dynamics being the sole words in the title so, any paper writing about eco-evolutionary dynamics can use that citation to “fill in the citation box” after their first sentence on the topic.  The second inflation factor he cites, is that citations beget citations. When “filling in the box”, authors tend to cite papers that other authors used to fill in the same box.  In other words, authors tend to be lazy and use what other people have cited in their introductions.  This is not something to be encouraged, as it can lead to people being wrongly attributed; I have raged against this practice in the past.  Stephen Heard over at Scientist See Squirrel reckons that his most original papers are cited less because they report research from “outside the box” and most people are working “inside the box”.  Dorothy Bishop over at Bishopblog suggests that the best way to bury your work is to put it in a book chapter in an edited book.

So, what about my stars and strays?  My most cited paper is indeed a review, and for an entomologist, being in that most prestigious of review journals, the Annual Review of Entomology, it is no surprise to me that it tops my top ten chart, with just over 1000 cites.  Incidentally, number 4 (Leather et al., 1999) and number 7 (Leather et al., 1989) in my top 10, are also reviews.  My second most cited paper (Leather, 1988), is also, I guess, a review of sorts, albeit very short, although I prefer to think of it as more of a synthesis cum speculation paper.

What about the duds, those that no-one cites, not even me.  If I ignore the most recent papers, those published this year (2018) and last 2017), as being unlikely to have had time to be read, let alone cited, then all my zero papers are either editorials or commentary papers (e.g. Leather, 2014).  Don’t let yourself be fooled by the hope that a commentary paper, even with a sexy title and published in a top-notch journal will get cited.  My effort in Journal of Animal Ecology in early 2015 being a prime example, even the magic words, “climate change” failing to elicit a single citation to date (Leather (2015).

It is hard to see a pattern in my other lesser cited papers, they don’t seem to be markedly different from my more frequently cited papers, being published in my usual journals and covering the same subject matter, aphids, agricultural and forest pests and biological control in the main.  I confess to being very disappointed in the low number of citations to my aphid cannibalism paper (Cooper et al., 2014) especially as it got a lot of media attention, but I guess it falls into the too original box, not many people work on aphid cannibalism 😊

Sadly, it seems that Steve Heard is right, despite the journal blurbs, we don’t value originality, and the message for both journal editors and authors, is clear, if you want citations, publishing reviews and sticking to well ploughed fields is the safest bet.

References

Cooper, L.C., Desjonqueres, C. & Leather, S.R. (2014) Cannibalism in the pea aphid, Acyrthosiphon pisum. Insect Science, 21, 750-758.

Leather, S.R. (1988) Size, reproductive potential and fecundity in insects – things aren’t as simple as they seem. Oikos, 51, 386-389.

Leather, S.R. (2014: Modifying glucosinolates in oilseed rape – Giamoustaris & Mithen (1995): a top-twenty paper in the Annals of Applied Biology. Annals of Applied Biology, 164, 318-319.

Leather, S.R. (2015) Title: Onwards and upwards – aphid flight trends follow climate change. Journal of Animal Ecology, 84, 1-3.

Leather, S.R., Walters, K.F.A. & Dixon, A, F.G. (1989) Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum-padi (L) (Hemiptera, Aphididae), in Europe – a study and review.  Bulletin of Entomological Research, 79, 345-360.

Leather, S.R., Day, K.R. & Salisbury, A.N. (1999) The biology and ecology of the large pine weevil, Hylobius abietis (Coleoptera: Curculionidae): a problem of dispersal? Bulletin of Entomological Research, 89, 3-16.

 

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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 1st 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 honeydewTransactions 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 activitiesAnnals 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 5th 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

 

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Pick and mix 18 – odds and ends from the web

The illegal orchid trade and its implications for conservation

On choosing titles for papers that actually tell you what they are about

When museums get it wrong, holiday booze or exhibit?

How earwing wings inspired a robotic gripper

What spiders can teach us about ecology

More bad news on the huge decline in numbers of insects and birds, this time in France

Manu Saunders is convinced that robotic bees will not be a success – what do you think?

An important report about the pollinator deficit from the Cambrigde Institute for Sustaianability Leadership

Great advice from Steve Heard on to rewrite your often-used methods and materials to avoid charges of plagiarism and copyright infringement

Are universities in loco parentis?

 

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Is there a place for humour in a scientific presentation?

Over at Ecological Rants, Charley Krebs recently wrote about and listed some very sensible and simple rules for giving a good lecture which are exactly the same things I tell my students when I give my lecture about basic presentation skills.  I do, however, also give some other hints and tips to help them give good talks and lectures.

Academics, with a few rare exceptions, are not, as a rule, stand-up comics; although, we are all, to some degree, performers. That said, there is, as I tell my students, definitely a place for humour in lectures and presentations.  The secret is making sure that it is appropriate and amusing. My first bit of advice, which I also take, is to avoid the supposedly, subtle scripted joke or play on words.  You have all sat in that lecture where the speaker very obviously works in a joke, and then the dead give-away, the expectant pause for the laugh, that is invariably either met by massed groans or a stony silence.  If you do feel the need to tell a joke per se, be upfront about it and say, “that reminds me about the…”.  It won’t be any funnier and you probably won’t get a round of applause, but hey, at least one person might laugh.

Far better is to go for the self-deprecating anecdote.  Your audience will be more sympathetic, and even if they are laughing at you, you will know that it is genuine 😊  I usually tell stories from  my working life and sometimes from my childhood. Something personal and shared, as long as it is in good taste, is always a good way to lighten a lecture and help your listeners remember a salient fact.

The thing to avoid at all costs is the careless, off the cuff comment, something that seems a great idea at the time and when without thinking, you let your mouth take over from your brain.  I speak, well write, from bitter experience.  In 1997, the 19th Symposium of the Royal Entomological Society was held in Newcastle from the 10th-11th September.  The subject of the symposium was Insect Populations and I had been invited to give the plenary address on the less than exciting subject of how qualitative changes in individual insects affects their population dynamics (Leather & Awmack, 1998).  I had a 45-minute slot and I must confess that after thirty minutes I was struggling.  Even I was finding the subject matter a bit dry, and I was desperately thinking of something to add a bit of life and colour to the talk.  I had just reached the section about lifespan when in view of an event that had happened a few days earlier, August 31st to be precise, I had what I thought was a brilliant idea, and these fatal words issued from my mouth “Death comes to us all as Princess Diana has just found out” There was a massed gasp from the audience, and then, if I had, had a pin to let go, you would have been able to hear it drop!

I use this story as an example of what not to do when I give my lecture on how to give a talk.  It always raises a laugh, albeit a shocked one 😊

My faux pas was certainly memorable.  Ten years later I was invited to give the plenary at Ento’07 in Edinburgh; the chair of the session on introducing me, pointedly made a reference to my infamous plenary of 1997 😊

Reference

Leather, S.R. & Awmack, C.S. (1998) The effects of qualitative changes of individuals in the population dynamics of insects. Pp 187-204 [In] Insect Populations in Theory and in Practice (eds. J.P. Dempster & I.F.G. McLean), Kluwer Academic Publishers, Dordrecht, Boston, London.

 

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Not all aphids grow up to be aphids – the enemy within

It has been said that if aphids had their own way and unlimited resources the world as we know it would be 149 km deep in the cute little beasts (Harrington, 1994 ). Last year I wrote about how predators that feed on aphids, although useful, don’t really cut the mustard when it comes to keeping them in check and suggested that their host plants played a major role in keeping aphids from taking over the World.  While they do play an important part in keeping aphid populations under control, and are aided and abetted by aphid specific predators, there are, however, some much more efficient aphid-specific natural enemies out there.  They may be less conspicuous than the brightly coloured ladybirds that we often see munching their way through aphid colonies; public perception of their name may make people wince, but these beautiful and graceful creatures make sure that our appetite for salads and exotic vegetables out of season is satisfied safely and efficiently.  Their life cycles rival that of their prey, or should that be hosts, and entomologists fondly imagine that the film Alien was inspired by them 😊

I am, of course, talking about parasitic wasps, or parasitoids as they are more commonly known.  They are called parasitoids because unlike true parasites which generally speaking keep their hosts alive, insect victims of these wasps will, if successfully parasitized, die well before their non-parasitized relatives. In case you were wondering, the term parasitoid was coined by the Finnish Hemipterist, Odo Reuter (1913).  Aphids are not the only insects that are attacked by parasitoid wasps. The action of insect parasites has been known about for over two hundred years.  Erasmus Darwin, grandfather of the more famous Charles, noted that Ichneumonid wasps parasitised cabbage white butterfly caterpillars and so should be encouraged by gardeners (Darwin, 1800).  This is not the only early mention of parasitic insects in this context; Wheeler (1928), points out that back in the 1850s, two Italian entomologists, Camillo Rondani and Vittore Ghiliana also suggested the use of parasitic insects as biological control agents.  Aphid pests of glasshouse crops originally controlled mainly by predators (van Lenteren & Woets, 1988) are now routinely controlled by the application of commercially produced Braconid and Chalcid wasps (Boivin et al., 2012; van Lenteren, 2012).

Three commonly used aphid parasitoid biological control agents in action. Images from http://biologicalservices.com.au/products/aphelinus-2.html and https://www6.inra.fr/encyclopedie-pucerons/Especes/Parasitoides/Braconidae-Aphidiinae/Praon-volucre

When people think of Hymenoptera, they tend to think of bees, Vespid wasps and ants as being the most important and abundant.  They are very much mistaken.  The Parastica, or parasitoid wasps, are, by a huge margin, the most speciose and abundant section of

Parasitoids clearly dominate the Hymenopteran fauna of the British Isles (Many thanks to Natalie Dale-Skey of the NHM for permission to use this).

the Hymenoptera both in the UK and elsewhere

In the tropics the parasitoids are even more dominant. Data from Gaston et al., (1996).

Once parasitized, the egg(s), unless they are encapsulated by the aphid ‘immune’ system, hatch and begin to feed on the internal tissues of their, presumably, unsuspecting aphid host.  The parasitoid larvae avoid feeding on vital parts of the aphid, so that it can continue to grow and develop and provide food for the parasitoid, until the parasitoid is ready to pupate. Once the parasitoid is ready to pupate it delivers the coup de grace putting the aphid out of its misery and allowing the formation of the ‘mummy’ in

The three most common types of aphid mummies.  Images from http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavershttp://biologicalservices.com.au/products/aphelinus-2.html and https://farm1.static.flickr.com/327/18532751584_becc0e56e9_b.jpg respectively.

which the parasitoid completes its development before sawing its way out to emerge as a winged adult ready to seek out new hosts, leaving a characteristic neat circular hole in mummy case. In case you were wondering why the mummy of Praon volucre looks like it is sitting on a plate, this because, unlike the other aphid parasitoids, the final instar cuts its way out of the bottom of the aphid and spins its cocoon externally underneath the remnants of the aphid, hence the ‘plate’ (Beirne, 1942).

And out she comes; emerging parasitoid – http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers

 

Lysiphelbus testaceipes  Photo by J.K.Clark, University of California Statewide IPM Project

Once an aphid, now a hollow mummy; note the neat emergence holes.  Aphid parasitoids are very much tidier than the parasitic lifeform in the classic film Alien 🙂

Another aspect of their life style that makes parasitoids a breed apart from true parasites, is that as well as using aphids as egg laying sites for their larvae, the adults like to snack on them every now and then to help mature more eggs and to keep up their energy levels; sometimes quaintly described as predatism (Flanders, 1953).  Although the parasitoids can make feeding attacks at any time, they appear to feed first and then start laying their eggs (e.g. Collins et al., 1981).

Parasitoids are widely used as biological control agents in glasshouses and other protected environments as they are generally regarded as being more effective than predators (Debach & Rosen, 1991), although there is some support that generalist predators can play a significant part in biological control in the wider environment (Symondson et al., 2002; Gontijo et al., 2015).  That said, aphid parasitoids seem to be fairly host specific in that commercial companies offer specific parasitoid mixtures to control different aphid pest species e.g.  https://www.koppert.com/pests/aphids/product-against/aphipar/ [Note this is NOT an endorsement]. In fact it has been suggested that the relationship between aphids and their parasitoids can be used to clarify aphid taxonomic relationships (Mackauer, 1965). On the other hand, there are very few examples of monophagous aphid parasitoids, most being described as oligophagous (Stary & Rejmanek, 1981).   So given that there is a fair bit of evidence that the parasitoids attacking aphids do show some discrimination in their choice of hosts, how do they find them?

Parasitoids in general were originally thought to be “possessed of an unerring instinct that guided them in their search for hosts” but Cushman (1926) rebutted this idea pointing out that actually the parasitoids first home in on the habitat or food plant that their host lives in and then search for their host (Laing, 1937).   The parasitoids referred to by Cushman and Laing, are however, not parasitoids of aphids, attacking lepidopteran leaf miners and carrion feeding flies respectively, so you might perhaps think that aphid parasitoids could have a different strategy. Although habitat selection by parasitoids of lepidopteran larvae (Thorpe & Caudle, 1938) and sawfly larvae (Monteith, 1955), using olfactory cues of their host’s food plant was confirmed readily easily and early on, the situation with aphids was less clear cut. Manfred Mackauer for example, suggested that aphid parasitoids might be using visual cues, such as leaf deformities or damage to find their aphids hosts (Mackauer, 1965).  The breakthrough came when three cabbage loving entomologists from the USA used an olfactometer to first show that the Braconid parasitoid Diaeretiella rapae, responded positively to the odour of collards (what we in the UK call spring greens) and second to show a very strong preference for them to lay their eggs in the aphid Myzus persicae when it was feeding on crucifers rather than other host plants.  They attributed this to the presence of mustard oil, the chemical that gives cabbages their distinctive taste and suggested that once the aphid host plant was found then the parasitoids used visual cues to find their aphid victims (Read et al., 1970).  Six years later it was firmly established that parasitoids in general used olfactory cues both to locate the habitat of their host (long-range) and then a short-range to find and confirm the identity (contact chemicals) their insect hosts (Vinson, 1976).

It was thought that the aphid parasitoids were chemically ‘conditioned’ during their larval life within the aphid feeding on a host plant and that this influenced their adult host preferences (e.g. Sheehan & Shelton, 1989; Wickremasinghe & Van Emden, 1992).  These, and other similar results, seemed to support the Hopkins host selection principle (Hopkins, 1917) which states that adult preferences are learnt as larvae.  A very neat experiment by van Emden et al., (1996) proved this hypothesis wrong. They transferred aphid mummies from the plant on which they had been parasitized on to another host plant and this changed the preference of the emerging adult, seeming to suggest that this was how aphid parasitoids developed their host preferences.  Now comes the neat, and very tricky part; if however, the parasitoid pupae were removed (very carefully) from the mummy case and reared to adulthood in the absence of a host plant or mummy and kept in a glass tube, the emerging adults showed no preference for particular host plants, clearly showing that adult preferences were  not determined during larval development but ‘conditioned’ by exposure to the external skin of the aphid mummy on emergence (van Emden et al., 1996).  Using aphids reared on an artificial diet (Douloumpaka & van Emden, 2003) showed that the it was very likely that the mother parasitoid leaves a chemical cue in or around the egg(s) she lays and that this is later incorporated into the silk of the parasitoid pupa, thus inducing the host preference seen as an adult.

An additional twist to the story is that male and female parasitoids differ in their responses to odours.  Both sexes of Aphidius uzbekistanicus and A. ervi, parasitoids of cereal aphids in the UK, respond to plant odours, but only females respond to aphids (Powell & Zhi-Li, 1983).  Males of both species are, however, attracted to the odours of their respective females, suggesting the existence of a sex pheromone. The existence of a sex pheromone in aphid parasitoids had been suggested a few years earlier when it was shown that male D. rapae attempted to copulate with filter paper that had had female abdomens crushed on them (Askari & Alisha, 1979).  The existence of sex pheromones in aphid parasitoids has now been shown in several species (e.g. Decker et al., 1993; McNeil & Broduer, 1995).  Strangely, female parasitoids also respond to sex pheromones, but in their case, the sex pheromones of aphids.  It turns out that they ‘parasitise’ aphids in more than one way, they home in on their prey using the aphid sex pheromone and this enables them to find a suitable overwintering host (Hardie et al., 1991).  At other times of the year they also use other aphid indicators; several studies have shown that parasitoids use the presence of aphid honeydew to help them find their hosts (Budenberg, 1990; Bouchard & Cloutier, 1984; Gardner & Dixon, 1985).

Predators of aphids such as ladybirds use chemical markers to warn other ladybirds that they have laid eggs near aphid colonies, thus reducing the chances of cannibalism and competition (e.g. Oliver et al., 2006). Given that the eggs of aphid parasitoids are laid internally, they are in effect invisible, it would make sense if the parasitoids ‘marked’ their hosts in some way to avoid other parasitoids laying their eggs in an already parasitized aphid, superparasitism.  Sure enough, there is some evidence that some adult parasitoids can recognise aphids that already have larval parasitoids developing inside them although they don’t seem to be able to consistently recognise already parasitized aphids until some hours afterward (e.g. Cloutier et al., 1984).  In some cases, it seems that it is the aphid herself that prevents superparasitism by reacting more aggressively towards parasitoids after being attacked once (Gardner & Dixon, 1984) and also by the presence of dried siphuncular secretions on the aphid’s skin (Outreman et al., 2001).  The waxy secretion had an effect for up to a day or so after which the internal changes caused by the developing parasitoid larvae were enough to deter further oviposition attempts.

It is a good thing for the poor aphids that they have such a high reproductive rate, or they would truly be in dire straits.  On the other hand, as exemplified by the words of Jonathan Swift (1733),

“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em,
And so proceed ad infinitum

there are parasites of parasitoids, the hyperparasites, that help keep the numbers of parasitoids under control, and thus, indirectly, help aphids remain relatively abundant.

 

References

Askari, A. & Alisha, A. (1979) Courtship behavior and evidence for a sex pheromone in Diaeretiella rapae (Hymenoptera: Braconidae), the cabbage aphid primary parasitoid. Annals of the Entomological Society of America, 72, 79-750.

Beirne, B.P. (1942) Observations on the life-history of Praon volucre Haliday (Hym.: Braconidae), a parasite of the mealy plum aphis (Hyalopterus arundinis Fab.). Proceedings of the Royal Entomological Society of London, Series A, General Entomology, 17, 42-47.

Boivin, G., Hance, T. & Brodeur, J. (2012) Aphid parasitoids in biological control.  Canadian Journal of Plant Science, 92, 1-12.

Bouchard, Y. & Cloutier, C. (1984) Honeydew as a source of host-searching kairomones for the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae).  Canadian Journal of Zoology, 62, 1513-1520.

Budenberg, W.J. (1990) Honeydew as a contact kairomone for aphid parasitoidsEntomologia experimentalis et applicata, 55, 139-148.

Cloutier, C., Dohse, L.A. & Bauduin, F. (1984) Host discrimination in the aphid parasitoid Aphidius nigripes. Canadian Journal of Zoology, 62, 1367-1372.

Collins, M.D., Ward, S.A., & Dixon, A.F.G. (1981) Handling time and the functional response of Aphelinus thomsoni, a predator and parasite of the. Journal of Animal Ecology, 50, 479-487.

Cushman, R.A. (1926) Location of individual hosts versus systematic relation of hots species as a determining factor in parasitic attack. Proceedings of the Entomological Society of Washington, 28, 5-6.

Darwin, E. (1800) Phytologia: or The Philosophy of Agriculture and Gardening. P. Byrne, Grafton Street, London.

Debach, P. & Rosen, D. (1991) Biological Control by Natural Enemies, Cambridge University Press, New York.

Decker, U.M., Powell, W. & Clark, S.J. (1993) Sex pheromone in the cereal aphid parasitoids Praon volucre and Aphidius rhopalosiphiEntomologia experimentalis et applicata, 69, 33-39.

Douloumpaka, S. & van Emden, H.F. (2003) A maternal influence on the conditioning to plant cues of Aphidius colemani Viereck, parasitizing the aphid Mysuze persicae SulzerPhysiological Entomology, 28, 108-113.

Flanders, S.E. (1953) Predation by the adult Hymenopteran parasite and its role in biological control. Journal of Economic Entomology, 46, 541-544.

Gardner, S.M. & Dixon, A.F.G. (1984) Limitation of superparasitism by Aphidius rhopalosiphi: a consequence of aphid defensive behaviour. Ecological Entomology, 9, 149-155.

Gardner, S.M & Dixon, A.F.G. (1985) Plant structure and foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae).  Ecological Entomology, 10, 171-179.

Gaston, K.J., Gauld, I.D. & Hanson, P. (1996) The size and composition of the hymenopteran fauna of Costa Rica.  Journal of Biogeography, 23, 105-113.

Griffiths, D.C. (1960) The behaviour and specificity of Monoctonus paldum Marshall (Hym., Braconidae), a parasite of Nasonovia ribis-nigbi (Mosley) on lettuce. Bulletin of Entomological Research, 51, 303-319.

Hardie, J., Nottingham, S.F., Powell, W. & Wadhams, L.J. (1991) Synthetic aphid sex pheromone lures female parasitoids.  Entomologia experimentalis et applciata, 61, 97-99.

Harrington, R. (1994) Aphid layer. Antenna18, 50-51.

Hopkins, A.D. (1917) Contribution to discussion.  Journal of Economic Entomology, 10, 92-93.

Holler, C. (1991) Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments and sex pheromone specificities (Hymenoptera, Braconidae, Aphidiinae. Systematic Entomology, 16, 15-28.

http://www.biologicalcontrol.info/aphid-primary-and-hyperparasitoids.html

Laing, J. (1937) Host-finding byinsect parasites 1. Observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescensJournal of Animal Ecology, 6, 298-317.

Mackauer, M. (1965) Parasitological data as an aid in aphid classification. Canadian Entomologist, 97, 1016-1024.

McNeil, J.N. & Brodeur, J. (1995) Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripesJournal of Chemical Ecology, 21, 959-972.

Monteith, L.G. (1955) Host preferences of Drino bohemica Mesn. (Diptera; Tachnidae) with particular reference to olfactory responses.  Canadian Entomologist, 87, 509-530.

Oliver, T.H., Timms, J.E.L., Taylor, A. & Leather, S.R. (2006) Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks. Bulletin of Entomological Research, 96, 25-34.

Outreman, Y., Le Ralec, A., Plantegenest, M., Chaubet, B, & Pierre, J.S. (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology, 47, 339-348.

Powell, W. & Zhi-Li, Z. (1983) The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants.  Physiological Entomology, 8, 439-443.

Reuter, O.M. (1913). Lebensgewohnheiten und Instinkte der Insekten (Berlin: Friendlander).

Stary, P. & Rejmanek, M. (1981) Number of parasitoids per host in different systematic groups of aphids: The implications for introduction strategy in biological control (Homoptera: Aphidoidea; Hymenoptera: Aphidiidae). Entomologica Scandinavica, Suppl. 15, 341-351.

Riley, W.A. (1931) Erasmus Darwin and the biologic* control of insects. Science, 73, 475-476.

Sheehan, W. & Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae).  Journal of Insect Behavior, 2, 743-759.

Symondson, W.O.C., Sunderland, K.D., & Greenstone, M.H. (2002) Can generalist predators be effective bicontrol agents? Annual Review of Entomology, 47, 561-594.

Thompson, W.R. (1930) The principles of biological control. Annals of Applied Biology, 17, 306-338.

Thorpe, W.H. & Caudle, H.B. (1938) A study of the olfactory responses of insect parasites to the food plant of their host.  Parasitology, 30, 523-528.

Van Emden, H.F., Spongal, B., Wagner, E., Baker, T., Ganguly, S. & Douloumpaka, S. (1996) Hopkins’ ‘host selection principle’, another nail in its coffin.  Physiological Entomology, 21, 325-328.

Van Lenteren, J.C. (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57, 1-20.

Van Lenteren, J.C. & Woets, J. (1988) Biological and integrated control in greenhouses.  Annual Review of Entomology, 33, 239-269.

Vinson, S.B. (1976) Host selection by insect parasitoids.  Annual Review of Entomology, 21, 109-133.

Wheeler, W.M. (1922). Social life among the insects: Lecture II. Wasps solitary and social. Scientific Monthly, 15, 68-88.

Wheeler, W.M. (1928) Foibles of Insects and Men.  Alfred Knopf, New York

Wickremasinghe, M.G.V. & Van Emden, H.F. (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology, 17, 207-304.

*This is how he spelt it; not a mistake on my part J

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Pick and mix 17 – gleanings from the web

A new approach to weed control?

A very personal and accessible paper about a rare butterfly by Nick Haddad

Why conserving species is important – warning for entomologists, there are a lot of vertebrate pictures 🙂

We need to conserve entomologists too

How some German cities are encouraging organic food gardens

George Monbiot admits that he was wrong to advocate global veganism; a great read but note that he has since qualified his view somewhat

And here is an article about George Monbiot’s controversial views about rewilding nature reserves and National Parks

Moving account of the life of the last Carolina parakeet that went extinct a century ago

A fun post from Kelly Jowett about filming a beetle larva

An interesting article about the harm done to Paris by modern architecture – Personally I think London has suffered more than Paris

 

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Inspiring the next generation of entomologists?

In the last couple of weeks, I have had the privilege to be involved in two different types of outreach involving the younger generation.  The first was Skypeascientist, which I came across via a blog post by Amy Parachnowitsch on Small Pond Science. Amy was so enthusiastic about it that I couldn’t resist signing up, to what is a great idea; in their own words “Skype a Scientist matches scientists with classrooms around the world! Scientists will skype into the classroom for 30-60 minute Q and A sessions that can cover the scientist’s expertise or what it’s like to be a scientist. We want to give students the opportunity to get to know a “real scientist”, and this program allows us to reach students from all over the world without having to leave the lab!” My first, and so far only, but hopefully not my last match was with a small primary school in the Cumbrian fells.  We had a bit of trouble with getting Skype working to begin with, but once contact was established I was subjected to some great, and in a couple of instances, tough questioning; what are the mots abundant insects in the world for one.  We covered what I did, why I did it and how I got started, as well as questions like the what is the most dangerous insects in the world, had I found any new insects, where had I been to study insects,  and from one little joker “have you ever had ants in your pants?”.  All in all, a very positive and enjoyable session and one, that I hope will result in at least one future entomologist, although sadly, by the time he or she arrives on our soon to start new entomology undergraduate degree, I will be long retired

The second outreach event was the Big Bang Fair held in Birmingham.  I participated in this last year and having enjoyed it so much, volunteered to help on two of the days; the fact that one of the days coincided with a deadly boring committee meeting that I would have had to attend otherwise, was purely coincidental 😉 If you’ve never heard of it, the Big Bang UK Young Scientists and Engineers Fair is the UK’s largest celebration of science, technology, engineering and maths, for young people, and is the largest youth event in the UK. The fair takes place annually in March, and was first run in 2009.  We, the Royal Entomological Society and Harper Adams University, first attended it last year, when a former student of mine, Fran Sconce, now Deputy Director of Outreach at the Royal Entomological Society, convinced us that it was a great event with which to become involved and to showcase our favourite science, entomology.  Fran was in charge this year too and did a sterling job as did the many volunteer demonstrators, drawn from among our current MSc entomologists and former students now doing PhDs.  They all did a fantastic job and I was hugely impressed by them all.

This was one of those events where the pictures tell the story but there were a few things that struck me.  First, I was surprised at how many of the teenage boys were afraid and disgusted by the thought of touching insects, the girls on the other hand, in the main were easier to win over to the concept.  When I was a teenager, now many years ago, it was the other way around.  Too much time spent indoors playing ‘shoot them up’ games perhaps might explain this, but perhaps that is too simple a view? Conversely pre-teens of both sexes seemed to respond in the same way, and overall were much easier to convince that it was safe and enjoyable to hold an insect.  Sadly, this seems to point to some anti-insect (maybe even Nature) ‘conditioning’ happening in young people once they leave primary education. Second, I was very surprised by how many times I was asked if the insect would bite them and/or was dangerous.  As I pointed out many times, “Would I be holding them and offering to let you hold them if they did and were?”  That said, I was very pleased that out exhibit attracted so much positive attention.  Some children made a lot of return visits 😊

 Now over to the pictures, which show the diversity of the young and older folk who were entertained and enthralled by our hard-working insects and volunteers.

 

One of the current MSc Entomology students and also a Royal Entomological Society Scholar, Brinna Barlow, demonstrating that you don’t have to be old, bearded and male to be an entomologist.

The First Day Team – the old and the new

A hive of activity at the entomology exhibit

 

Swarms of future entomologists?

Visitors and volunteers buzzing with enthusiasm

Some of our volunteers, Entomology MSc students past and present

 

Our new Entomology lecturer, Heather Campbell, showing that although she is an ant specialist, leaf insects are also cool.

Yours truly demonstrating that quite a few entomologists are oldish, greyish, bearded and male, but remember, we were young once 🙂

Bearded and male, but definitely younger

And finally, without the enthusiasm, dedication, and hard work of Fran Sconce, and the willingness of our current MSc Entomologists to give up some of their exam revision time, our exhibit would have been much diminished.  It was a privilege to stand alongside them all.

The Director and star of the show, Fran Sconce, with one of her co-stars, both fantastic ambassadors for entomology.

 

Post script

This post has the dubious distinction of being the first one I have ever posted while at sea; the Dublin to Holyhead ferry, m.v. Ulysses to be precise 😊

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