Malham in the Sun – introducing entomology to budding ecologists

Last year I wrote about my experience of being a tutor at the British Ecological Society’s Undergraduate Summer School at the Malham Tarn Field Studies Council site. I really enjoyed myself and also found it very refreshing to have the opportunity to interact with 50 bright young proto-ecologists. It appears that the students also enjoyed themselves as I was invited back this year to repeat my performance. I was very happy to accept the offer, after all, any chance to visit the county of my birth (Yorkshire) is not to be sneezed at and with the added bonus of being able to talk about entomology to a new audience thrown in I would have been made to turn it down. Thus it was that I headed up the dreaded M6 motorway on a sunny Monday afternoon (July 18th) with joy in my heart and a car boot full of entomological equipment and identification keys. The M6 did not disappoint and I spent an hour sweltering in the summer sunshine very slowly (very, very slowly) making my way through the inevitable road works. Luckily, being one of those people who likes to arrive early for appointments, I was only fifteen minutes late collecting my trusty assistant, Fran Sconce, from the very picturesque Settle Station and then heading up on to the FSC Malham Tarn site.

Malham 1
The weather on arrival was in marked contrast to last year.

We unloaded the car and just had time to set up 35 pitfall traps before heading in for the evening meal after which the students went on a long walk to Malham Cove.

Malham 2

The long walk

 I walked part of the way back with them but turned back in time to get to the bar:-)  for a very welcome drink, before retiring to bed.

The next day was even hotter, and we spent the morning setting up the labs and teaching areas.

DSCF7290

This year, as well as the fifty undergraduates we had ten sixth form students from several different schools in London.  Last year interacting with a class of fifty had posed certain difficulties, so this year we divided the students into two groups and ran the session twice, once on the Tuesday afternoon and then again on the Wednesday morning.  This worked extremely well and meant that Fran and I and the PhD mentors assigned to us, were able to spend much more time with each student and also meant that we were not as rushed off our feet as we would have been otherwise.  So a win/win outcome, although I did have to give the same lecture twice in 24 hours which was an interesting experience.  On the Tuesday afternoon, I started with my lecture on why entomology is important and an overview of the insects.

Malham 3

I seem to have done a lot of arm waving

Malham

We then went outside and I demonstrated sampling methods while the students baked under, a by now, extremely hot sun, before sending them off to empty and reset the pitfall traps and collect other insects using nets and beating trays.

Malham 5

Being cruel to trees

 

Malham 6  Malham 4

Some of the stars of the day

 

Then it was back to the labs to identify the catches before the evening meal and refreshing drink or two in the bar*.   After the bar closed we had the fluorescent beetle extravaganza.  Last year I demonstrated the use of fluorescent dust on one hapless carabid beetle.  This year I used ten, and two different coloured dusts.  The beetles were then released after dark in

Malham 7

Fluorescing carabids

the courtyard outside the teaching labs where they were photographed fluorescing colourfully under my UV flashlight, as I ‘chased’ them around the arena, much to the delight of the watching students.

As the weather forecast was not very good for the Wednesday morning, we did the insect sampling first, in case the forecast rain was as heavy as predicted.  As it turned out, apart from a short sharp shower, whilst I was demonstrating sampling methods, the sun came out and there were plenty of insects to collect before I did my lecture and we headed in to the labs for another ID session.  All too soon the session was over, and Fran and I, after a hasty lunch, drove back down to Shropshire.

I think that the BES summer school is a superb idea and that the students get a great deal from it.  I thoroughly enjoyed it and hope that I get the chance to be involved in any future summer schools.  I was also greatly impressed by the 6th formers who certainly seemed to enjoy my entomology session, one of whom produced this excellent drawing.

Malham 8

Much better than anything I could draw

For those of you on Twitter #bestug16 will give you a flavour of the whole week.

Malham 9

Glorious Yorkshire

 

*staffed that evening by the son of my best friend from school!

 

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Roundabouts – so much more than traffic-calming devices

Roundabout1

I have often been asked why I work on roundabouts, or urban green spaces, if you want to sound more scientific and ecological. Roundabouts to me are not just traffic-calming devices.

Roundabout2

They are a teaching tool,

 

 

Roundabout3

a research programme

 

Roundabout4

and a source of amusement and wonder.

 

Roundabout5

They are islands of calm among a sea of traffic, a haven for wildlife amidst a tarmac and concrete jungle.

Hook of Holland

or just plain fun!

So, next time you are waiting to enter a roundabout, don’t just think of it as an impediment (or aid) to your journey, but as a haven of wild-life, an urban nature reserve

Roundabout6

or even as a work of art, especially if you are in France:-)

 

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Getting a buzz with science communication – Reflections on curating Realscientists for a week

My week on Realscientists was a direct result of National Insect Week, a biennial event organised by the Royal Entomological Society (RES) to bring the wonders of entomology to a wider audience*. I had never thought about being a curator for Realscientists although I have followed them for some time.  Back in February however, one of my PhD students who has been involved with National Insect Week on more than one occasion, suggested that I might apply to curate RealScientists during National Insect Week as the RES Director of Outreach, Luke Tilley, was hoping to be on Biotweeps during National Insect Week as well.  To make sure that I had no excuse to forget to do it, she very helpfully sent me the link to the Realscientists web site and instructions on how to apply:-)

Duly briefed, I contacted Realscientists and to my surprise and slight apprehension, was given the slot I had asked for, the week beginning 19th June.  As my curatorial stint drew closer I began to worry about what I was going to tweet about and how to fit it into my day-to-day activities.

I made a list of twenty pre-planned Tweets to give me an outline script to work from. I managed to include all but one into my week as curator, the one about why you should want to work in entomology.

RS1

The twenty tweet list

I felt that my whole week was addressing this point so there was no need to belabour the point any more.  I also received an email from Realscientists with a Vade Mecum of how and what to tweet.  I was somewhat concerned by the section on how to deal with trolling, but I needn’t have worried, as far as I could tell I received no overt abuse**.

The big day approached, which as my actual launch was at Sunday lunchtime caused some slight logistical problems, but easily solved by making lunch a bit later than usual. As it was a Sunday I basically kept it light, introduced myself and tweeted a few insect factoids and pictures, including some great images from van Bruyssels The Population of an Old Pear Tree.  I have my own hard copy of the 1868 translated edition, but if you want to read it on-line it is available here.

RS2a

From van Bruyssel – The Population of an Old Pear Tree

It is definitely worth a read.

I also had to make a decision about how much time I was going to spend Tweeting. The previous curator had only done about 10-15 tweets a day, which is what I usually do.  The curator before her, however, had done considerably more.  As my stint as curator coincided with National Insect Week and as my contract with my university does actually specify that I do outreach***, I felt that I could justify several hours a day to it and that is what I did, and managing to fit quite a bit of the day job in between.

In between tweeting images and fantastic insect facts I tried to get some important messages across to my audience.  I started with what some might  term a “conservation rant”, basically bemoaning the fact that although insects make up the majority of the animal kingdom, conservation research and funding is very much biased toward the vertebrates, largely those with fur and feathers.  I also pointed out that most statements about how we should go about conservation in general is based on this unbalanced and not very representative research.  Taxonomic chauvinism has annoyed my for a long time:-)

RS3

That rant over I introduced my audience to the work our research group does, biological control, chemical ecology, integrated pest management, agro-ecology and urban ecology and conservation. Our use of fluorescent dust and radio tagging to understand insect behaviour aroused a lot of interest and comment.

 RS4

Using alternative technology to understand vine weevil behaviour.

RS5

The glow in the dark sycamore aphid was also very popular

 

Midweek I translated one of my outreach talks to Twitter and in a frenzy of Tweets introduced the world to Bracknell and the biodiversity to be found on its roundabouts and how an idea of how to teach locally relevant island biogeography and conservation, turned into a 12 year research project.

RS6

How teaching led research – the Bracknell roundabout story.

In between these two main endeavours, I tweeted about the influences that entomology has had on art, literature, popular culture, religion, medicine, engineering, advertising, economics, medicine , fashion and even advertising, using a variety of images.

RS7

Our new insect-inspired smoke detector attracted a lot of love and envy.

I even composed a haiku for the occasion

Six-legged creatures;

Fascinating and diverse,

Beautiful insects

 

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I have been an entomologist for a long time.

and told the story of my life-long love of insects, incidentally revealing some of my past hair-styles and exposing my lack of interest in sartorial elegance:-)

My overall message for the week was, and hopefully I got this across, is that we should be much

RS9

more aware of what is under our feet and surrounding us and of course, that aphids are not just fantastic insects

RS10

My final tweet

but also beautiful animals.

Giant Myzus

Model Myzus persicae that I recently met in the Natural History Museum

And finally, would I do it again? Yes most definitely. I ‘met’ a lot of new and very interesting people and had some really good ‘conversations’.

 

References

Harrington, R. (1994) Aphid layer.  Antenna, 18, 50-51.

Huxley, T.H. (1858) On the agamic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society of London, 22, 193-219.

Leather, S. R. (2009). Taxonomic chauvinism threatens the future of entomology. Biologist 56, 10-13.

 

 

*I was one of the original ‘founders’ of National Insect Week so have always tried to be involved in some way with the event.

**or I am so thick-skinned I didn’t notice it:-)

***or as Harper Adams University quaintly terms it, “reach out”

 

 

 

 

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Data I am never going to publish in peer-reviewed journals

I have got to that stage in my career where retirement is no longer a distant speck on the horizon; something that 20 years ago I never even thought about, but which now I am actually looking forward to reaching. Don’t get me wrong, I have, in the main, enjoyed what I have been paid to do for the last 40 years, but I’m looking forward to a change of pace and a change of priorities. I’m not planning on leaving entomology and ecology, or putting my collecting equipment in a cupboard, throwing my field guides away and burning all my reprints in a huge bonfire. Nor do I plan on deleting my EndNote™ files and database when I retire to our house in Languedoc-Roussillon to sit next to the pool with a never-emptying glass of red wine and gently pickle myself in the sun*. I’m just looking forward to approaching it in a different way; my plan is to stop initiating the writing scientific papers, but instead to expand on the outreach, to blog more and to write books for a wider audience. I want to spread the joys and wonders of entomology to the world, and hopefully, supplement my pension a bit to make sure that I can keep that glass filled with red wine and heat the swimming pool in the winter:-)

I’m planning a gradual retirement, a slow(ish) canter towards the day (September 30th 2020) when I finally vacate my university office and move full-time into my converted attic in the Villa Lucie surrounded by my books and filing cabinets with a superb view of the mountains.

View

The view from my study to be – I will have to stand up to see it, but exercise is good for you:-)

I have already reached a number of milestones, I took on my last ever PhD student (as Director of Studies) this month (June 7th) and submitted my final grant application as a PI (June 10th).

Grant

I must admit that it is a bit of funny feeling, but a remarkably rewarding one in many ways. I look at my former colleagues who have already retired productively and enjoyably, and I’m envious, so I know that I am making the right decision despite the slight feeling of apprehension. I now have a dilemma. As Jeff Ollerton points out, when you have been around a while, in my case it is almost 40 years since I started my PhD**, you build up a substantial amount of data, especially, if as I have, you have supervised over 150 undergraduate research projects, an equal number of MSc research projects and over 50 PhD students. Much of these data are fragmentary, not significant or even lost (sadly when I moved from Imperial College, they threw away the hard copies of my undergraduate projects, although I can remember what some of the lost data were about). My ten year sycamore and bird cherry aphid field study from my time in Scotland (1982-1992) remains largely unpublished and my huge twenty year sycamore herbivores data set from Silwood Park (1992-2012) is in the same boat, although parts of the data are ‘out on loan’ to former students of mine and I hope will be analysed and published before I retire.

This leaves however, the data, some of it substantial, which I would like to see the light of day, e.g. a whole set of rabbit behaviour data that I collected one summer with the help of an undergraduate and MSc student, which surprisingly revealed novel insights. Other data, perhaps not as novel, may be of interest to some people and there is a whole bunch of negative and non-significant data, which as Terry McGlynn highlights over on Small Pond Science, does not necessarily mean that it is of no use.   I have, as an example of fragmentary, not entirely earth-shattering data, the following to offer. Whilst monitoring aphid egg populations on bird cherry and sycamore trees, in Scotland between 1982 and 1992, I occasionally sampled overwintering eggs of Euceraphis betulae, on some nearby birch (Betula pendula) trees and of Tuberculoides annulatus, on an oak tree (Quercus robur) in my back garden in Peebles.

As far as I know there are no published data on the overwintering egg mortality of these two aphids. Although novel for these two aphid species, the observation of the way the egg populations behave over the winter and the factors causing the mortality have already been described by me for another aphid species (Leather, 1980, 1981). I am therefore unlikely to get them published in any mainstream journal, although I am sure that one of the many predatory journals out here would leap at the chance to take my money and publish the data in the Journal of Non-Peer-Reviewed Entomology :-) I could of course publish the data in one of the many ‘amateur’ type, but nevertheless peer-reviewed journals, such as Entomologist’s Monthly Magazine, The Entomologist’s Record, The Entomologist’s Gazette or the British Journal of Entomology & Natural History, which all have long and distinguished histories, three of which I have published in at least once (Leather & Brotherton 1987, Leather, 1989, 2015), but which have the disadvantage of not being published with on-line versions except for those few issues that have been scanned into that great resource, The Biodiversity Heritage Library, so would remain largely inaccessible for future reference.

I thus offer to the world these data collected from four Betula pendula trees in Roslin Glen Nature Reserve in Scotland between 1982 and 1986. On each sampling occasion, beginning at the end of October, 200 buds were haphazardly selected and the number of eggs present in the bud axils recorded. Sampling continued until egg hatch began in the spring.

Graph

Figure 1. Mean number of eggs per 100 buds of the aphid Euceraphis betulae present on four Betula pendula trees at Roslin Glen Nature Reserve Scotland***.

The number of eggs laid on the trees varied significantly between years (F = 20.3, d.f. = 4/15, P <0.001) ranging from 12.75 eggs/100 buds in 1983-84 to 683 eggs/100 buds in 1986-87. Mortality occurred at a regular rate over the winter and ranged from between 60% in 1985-86 to 83 % in 1984-85, averaging out at 74% over the five-year study.

So in conclusion, no startling new insights, but just some additional data about aphid egg mortality to add to the somewhat sparse records to date (Leather, 1992). Perhaps it is time for me to write another review:-)

References

Leather, S.R. (1980) Egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 27, 96-97.

Leather, S.R. (1981) Factors affecting egg survival in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 30, 197-199.

Leather, S.R. (1986) Insects on bird cherry I. The bird cherry ermine moth, Yponomeuta evonymellus (L.). Entomologist’s Gazette, 37, 209-213.

Leather, S.R. (1989) Phytodecta pallida (L.) (Col.,Chrysomelidae) – a new insect record for bird cherry (Prunus padus). Entomologist’s Monthly Magazine, 125, 17-18.

Leather, S.R. (1992) Aspects of aphid overwintering (Homoptera: Aphidinea: Aphididae). Entomologia Generalis, 17, 101-113.

Leather, S.R. (2015) An entomological classic – the Pooter or insect aspirator. British Journal of Entomology & Natural History, 28, 52-54.

 

*although in light of the recent horrific BREXIT vote this may now not be as simple as it might have been😦

**I must confess that I haven’t actually published all the data that I collected during my PhD. I rather suspect that this will never see the light of day:-)

***Data from 1986-87 are not shown as their inclusion makes it very difficult to see the low years. I can assure you however, that the mortality rate shows the same patterns as the other years.

 

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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.

Solomon 1

Making sure that nobody could claim my copy of Population Dynamics

Solomon terms

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.

Tillyard

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.

Solomon combo

 

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.

 

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Not all aphids have the same internal biomes

Headline message for those of you too busy to read the whole thing

Aphids have mutualistic symbiotic bacteria living inside them, one set, the primary endosymbionts, Buchnera aphidicola are obligate, i.e. in normal circumstances, the aphid can’t live without them and vice versa. All aphids have them. The others, the secondary symbionts, of which there are, at the last count, more than seven different species, are facultative, i.e. aphids can survive without them and not all aphids have them or the same combination of them. These can help the aphid in many ways, such as, making them more resistant to parasitic wasps, able to survive heat stress better and helping them use their host plants more efficiently. Hosting the secondary symbionts may, however, impose costs on the aphids.

Now read on, or if you have had enough of the story get back to work :-)

Like us, aphids have a thriving internal ecology, they are inhabited by a number of bacteria or bacteria like organisms. The existence of these fellow travellers and the fact that they are transmitted transovarially, has been known for over a hundred years (Huxley, 1858; Peklo, 1912)*, although their role within the body of the aphids was not entirely understood for some time, despite Peklo’s conviction that they were symbionts and transferred via the eggs to the next generation. Some years later the Hungarian entomologist László Tóth** hypothesised that aphids because the plant sap that they feed on did not contain enough proteins to meet their demands for growth, must be obtaining the extra nitrogen they needed from their symbionts, although he was unable to prove this empirically (Tóth, 1940). This was very firmly disputed by Tom Mittler some years later, who using the giant willow aphid, Tuberolachnus salignus, showed that aphid honeydew and willow phloem sap contained the same amino acids (Mittler, 1953, 1958ab). It was not only aphidologists who were arguing about the nature and role of insect symbionts, as this extract from a review of the time makes clear,

It is not our purpose here to harangue on terminology; suffice it to say that we will use “symbiote” for the microorganism and “host” for the larger organism (insect) involved in a mutualistic or seemingly mutualistic association.” (Richards & Brooks, 1958).

Interestingly it is in this paper that they mention, using the term “provocactive” the use of antibiotics to create aposymbiotic individuals in attempts to prove that the symbionts were first bacteria, and second, benefiting their insect hosts. The concluded that there was enough evidence to suggest that the endosymbionts were involved in some way in the nutritional and possibly reproductive processes of the insects studied, mainly cockroaches. At the time of the review no similar work had been done on aphids. A few years later though, two American entomologists sprayed aphids with several different antibiotics and found that this caused increased mortality and reduced fecundity when compared with untreated ones (Harries & Mattson, 1963). Presaging its future dominance in aphid symbiont work, one of the aphids was the pea aphid, Acyrthosiphon pisum. Antibiotics were also shown to eliminate and damage the symbionts associated with Aphis fabae followed by impaired development and fecundity in the aphid itself adding yet more evidence that the symbionts were an essential part of the aphid biome (Ehrhardt & Schmutterer, 1966). There was, however, still much debate as to how the symbionts provided proteins to the aphids, and although light and electron microscopy studies confirmed that the symbionts were definitely micro-organisms (Lamb & Hinde, 1967; Hinde, 1971), the answer to that question was to remain unanswered until the 1980s although the development of aphid artificial diets (Dadd & Krieger, 1967) which could be used in conjunction with antibiotic treatments, meant that it was possible to show that the symbionts provided the aphids with essential amino acids (Dadd & Kreiger, 1968; Mittler, 1971ab).*** Although the existence of secondary symbionts in other Homoptera was known (Buchner, 1965), it was not until Rosalind Hinde described them from the rose aphid, Macrosiphum rosae, that their presence in aphids was confirmed (Hinde, 1971).   Of course it was inevitable that they would then be discovered in the pea aphid although their role was unknown (Grifiths & Beck, 1973). Shortly afterwards they were able to show that material produced from the symbionts was passed into the body of the aphid (Griffiths & Beck, 1975) and it was also suggested suggested that it was possible that the primary symbionts were able to synthesise amino acids (Srivastava & Auclair, 1975) and sterols (Houk et al., 1976) for the benefit of their aphid hosts (partners). By the early 1980s it was accepted dogma that aphids were unable to reproduce or survive without their primary symbionts (Houk & Griffiths, 1980; Ishikawa, 1982) and by the late 1980s that dietary sterols were provided by the primary symbionts (Douglas, 1988).

Symbionts

Primary symbiont (P) in process of dividing seen next to secondary symbionts (S) and mitochondrion (m) from Houk & Griffiths (1980).

Despite the huge amount of research and the general acceptance that the endosymbionts were an integral part of the aphid’s biome “The mycetocyte symbionts are transmitted directly from one insect generation to the next through the female. There are no known cases of insects that acquire mycetocyte symbionts from the environment or from insects other than their parents” (Douglas , 1989), their putative identity was not determined until 1991 (Munson et al., 1991), when they were named Buchnera aphidicola, and incidentally placed in a brand new genus. Note however, that like some aphids, B. aphidicola represents a complex of closely related bacteria and not a single species (Moran & Baumann, 1994). Research on the role of the primary symbionts now picked up pace and it was soon confirmed that they were responsible for the synthesis of essential amino acids used by the aphids, such as tryptophan (Sasaki et al., 1991; Douglas & Prosser, 1992) and that it was definitely an obligate relationship on both sides**** (Moran & Baumann, 1994).

Now that the mystery of the obligate primary endosymbionts was ‘solved’, attention turned to the presumably facultative secondary symbionts, first noticed more than twenty years earlier (Hinde, 1971)***** began to be scrutinised in earnest. Nancy Moran and colleagues (Moran et al., 2005) identified three ‘species’ of secondary bacterial symbionts, Serratia symbiotica, Hamiltonella defensa and Regiella insecticola. As these are not found in all individuals of a species they are facultative rather than obligate. The secondary symbionts were soon shown not to have nutritional benefits for the aphids (Douglas et al., 2006). They are instead linked to a whole swathe of aphid life history attributes, ranging from resistance to parasitoids (Oliver et al., 2003; 2005; Schmid et al., 2012), resistance to heat and other abiotic stressors (Montllor et al., 2002; Russell & Moran 2006; Enders & Miller, 2016) and to host plant use (Tsuchida et al., 2004; McLean et al., 2011; Zytynska et al., 2016).

And finally, Mittler (1971b) mentions the reddish colouration developed by aphids reared on some of the antibiotic diets and hypothesises that this may be linked to the symbionts. I have written earlier about aphid colour variants and the possibility that the symbionts may have something to do with it. The grain aphid, Sitobion avenae has a number of colour variants and it was suggested that levels of carotenoids present might have something to do with the colours expressed and that in some way this was controlled by the presence of absence of symbionts (Jenkins et al., 1999). More recently Tsuchida and colleagues in a series of elegant experiments on the ubiquitous pea aphid, have shown that the intensity of green colouration is dependent on the presence of yet another endosymbiont, a Rickettsiella (Tsuchida et al., 2010). The authors hypothesise that being green

Pea aphids colour

Elegant demonstration that in some strains of the pea aphid, green colour is a sign of an infection by Rickettsiella (Tsuchida et al., 2010).

rather than pink or red, may reduce predation by ladybirds as has been suggested before (Losey et al., 1997).

New secondary symbionts continue to be discovered and with each discovery, new hypotheses are raised and tested. It would seem that there is a whole ecology of secondary symbionts within the aphid biome waiting to be explored and written about (Zytynska & Weisser, 2016). What are you waiting for, but do remember to come up for air sometime and relate what you find back to the ecology of the aphids:-)

 

References

Buchner, P. (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience, New York.

Dadd, R.H. & Krieger, D.L. (1967) Continuous rearing of aphids of the Aphis fabae complex on sterile synthetic diet. Journal of Economic Entomology, 60, 1512-1514.

Dadd, R.H. & Krieger, D.L. (1968) Dietary amino acid requirements of the aphid Myzus persicae. Journal of Insect Physiology, 14, 741-764.

Douglas, A.E. (1988) On the source of sterols in the green peach aphid, Myzus persicae, reared on holidic diets. Journal of Insect Physiology, 34, 403-408.

Douglas, A.E. (1998) Mycetocyte symbiosis in insects. Biological Reviews, 64, 409-434.

Douglas, A.E. & Prosser, W.A. (1992) Sythesis of the essential amiono acid trypthotan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38, 565-568.

Douglas, A.E., Francois, C.M.L.J. & Minto, L.B. (2006) Facultative ‘secondary’ bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiological Entomology, 31, 262-269.

Ehrhardt, P. & Schmutterer, H. (1966) Die Wirkung Verschiedener Antibiotica auf Entwicklung und Symbionten Künstlich Ernährter Bohnenblattläuse (Aphis fabae Scop.). Zeitschrift für Morphologie und Ökologie der Tiere, 56, 1-20.

Enders, L.S. & Miller, N.J. (2016)Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid. Ecology & Evolution, 6, 818-829.

Griffiths, G.W. & Beck, S.D. (1973) Intracellular symbiotes of the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 19, 75-84.

Griffiths, G.W. & Beck, S.D. (1975) Ultrastructure of pea aphid mycetocystes: evidence for symbiote secretion. Cell & Tissue Research, 159, 351-367.

Harries, F.H. & Mattson, V.J. (1963) Effects of some antibiotics on three aphid species. Journal of Economic Entomology, 56, 412-414.

Hinde, R. (1971) The control of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae, and Macrosiphum rosae. Journal of Insect Physiology, 17, 1791-1800.

Houk, E.J. & Griffiths, G.W. (1980) Intracellular symbiotes of the Homoptera. Annual Review of Entomology, 25, 161-187.

Houk, E.J., Griffiths, G.W. & Beck, S.D. (1976) Lipid metabolism in the symbiotes of the pea aphid, Acyrthosiphon pisum. Comparative Biochemistry & Physiology, 54B, 427-431.

Huxley, T.H. (1858) On the agamic reproduction and morphology of Aphis – Part I. Transactions of the Linnean Society of London, 22, 193-219.

Ishikawa, H. (1978) Intracellular symbionts as a major source of the ribosomal RNAs in the aphid mycetocytes. Biochemical & Biophysical Research Communications, 81, 993-999.

Ishikawa, H. (1982) Isolation of the intracellular symbionts and partial characterizations of their RNA species of the elder aphid, Acyrthosiphon magnoliae. Comparative Biochemistry & Physiology, 72B, 239-247.

Jenkins,  R.L., Loxdale, H.D., Brookes, C.P. & Dixon, A.F.G. (1999)  The major carotenoid pigments of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae).  Physiological Entomology, 24, 171-178. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-3032.1999.00128.x/pdf

Lamb, R.J. & Hinde, R. (1967) Structure and development of the mycetome in the cabbage aphid, Brevicoryne brassciae. Journal of invertebrate Pathology, 9, 3-11.

Losey, J. E., Ives, A. R., Harmon, J., Ballantyne, F. &Brown, C. (1997). A polymorphism maintained by opposite patterns of parasitism and predation. Nature, 388, 269-272.

McLean, A.H.C., van Asch, M., Ferrari, J. & Godfray, H.C.J. (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B., 278, 760-766.

Mittler, T.E. (1953) Amino-acids in phloem sap and their excretion by aphids. Nature, 172, 207.

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

Mittler, T.E. (1958b) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). III The nitrogen economy. Journal of Experimental Biology, 35, 626-638.

Mittler, T.E. (1971a) Dietary amino acid requirements of the aphid Myzus persicae affected by antibiotic uptake. Journal of Nutrition, 101, 1023-1028.

Mittler, T.E. (1971b) Some effects on the aphid Myzus persicae of ingesting antibiotics incorporated into artificial diets. Journal of Insect Physiology, 17, 1333-1347.

Montllor, C.B., Maxmen, A. & Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea pahids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.

Moran, N. & Baumann, P. (1994) Phylogenetics of cytoplasmically inherited microrganisms of arthropods. Trends in Ecology & Evolution, 9, 15-20.

Moran, N.A., Russell, J.A., Koga, R. & Fukatsu, T. (2005) Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied & Environmental Microbiology, 71, 3302-3310.

Munson, M.A., Baumann, P. & Kinsey, M.G. (1991) Buchnera gen. nov. and Buchnera aphidicola sp. Nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. International Journal of Systematic Bacteriology, 41, 566-568.

Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences USA, 100, 1803-1807.

Oliver, K.M., Moran, N.A. & Hunter, M.S. (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences USA, 102, 12795-12800.

Peklo, J (1912) Über symbiotische Bakterien der Aphiden. Berichte der Deutschen Botanischen Gesellschaft, 30, 416-419.

Richards, A.G. & Brooks, M.A. (1958) Internal symbiosis in insects. Annual Review of Entomology, 3, 37-56.

Russell, J.A. & Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B, 273, 603-610.

Sasaki, T., Hayashi, H. & Ishikawa, H. (1991) Growth and reproduction of the symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum mainatained on artificial diets. Journal of Insect Physiology, 37, 749-756.

Schmid, M., Sieber, R., Zimmermann, Y.S. & Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology, 26, 207-215.

Srivastava P.N. & Auclair, J.L. (1975) Role of single amino acids in phagostimualtion, growth, and survival of Acyrthosiphon pisum. Journal of Insect Physiology, 21, 1865-1871.

Tóth, L. (1940) The protein metabolism of aphids. Annales Musei Nationalis Hungarici 33, 167-171.

Tsuchida, T., Koga, R. & Fukatsu, T. (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989.

Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., Simon, J. C. &Fukatsu, T. (2010). Symbiotic bacterium modifies aphid body color. Science 330: 1102-1104.

Zytynska, S. E. &Weisser, W. W. (2016). The natural occurrence of secondary bacterial symbionts in aphids. Ecological Entomology, 41, 13-26.

Zytynska, S.E., Meyer, S.T., Sturm, S., Ullmann, W., Mehrparvar, M. & Weisser, W.W. (2016) Secondary bacterial symbiont community in aphids responds to plant diversity. Oecologia, 180, 735-747.

 

Footnotes

*I should point out that although Huxley clearly described the structure and contents of the mycetocytes he had absolutely no idea what they were and what function, if any, they had. Despite the many authors who supported Peklo’s claim that the contents of the mycetocytes were bacteria he was still having to defend himself against detractors more than 50 years later (Peklo, 1953).

Peklo, J. (1953) Microorganisms or mitochondria? Science, 118, 202-206.

 

**not to be confused with the László Tóth who vandalised Michelangelo’s Pietà

***interestingly, although the existence of primary symbionts in aphids and their possible role in aphid nutrition was by then firmly established, my vade mecum as a student, Tony Dixon’s Biology of Aphids, makes no mention of them at all, although first published in 1973. The first edition of Aphid Ecology (1985) also by Tony Dixon, only devotes three quarters of a page to them, but by the second edition, published in 1998, they get a whole chapter to themselves.

Buchnera appears to have been ‘lost’ but replaced by a yeast like symbiont (Braendle et al., (2003).

Braendle, C., Miura, T., Bickel, R., Shingleton, A.W., Kambhampari, S. & Stern, D.L. (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PloS Biology, 1, e21. doi:10.1371/journal.pbio.0000021.

 

*****although Huxley’s description of the unknown structures that he saw in aphids in 1858, does seem to include secondary symbionts as well as the primary ones.

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Does naming your study animals introduce observer bias?

I think, that most, if not all entomologists, will confess to a bit of funding envy when talking with those of their colleagues who work with the “undeserving 3%”, the large charismatic mega-fauna and the modern dinosaurs. The terminology gives us away, although the evidence is overwhelmingly on our side (Leather, 2009).  As entomologists, particularly those of us working in the field, we are used to reporting numbers collected in the tens of thousands (Ramsden et al., 2014 ), if not the hundreds of thousands (Missa et al., 2009) and  even a short six-week study can result in the capture of thousands of ground beetles (Fuller, et al., 2008).  Naming our subjects, much as we love them, is not an option, even if we wanted to. Even behavioural entomologists counting individual flower visits by pollinators are used to dealing with hundreds of individuals.   In the laboratory, although numbers may be smaller, say tens, we still assign them alphanumeric codes rather than names, even though one might look forward to counting the number of eggs laid by the unusually fecund moth #17 or hope that aphid #23 will be dead this morning as she is becoming a pesky outlier for your mortality data:-)

Our colleagues who work with mammals in the field, seem however to adopt a different strategy. It appears quite common for them to name their animals as the following examples from Twitter make clear.

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From her dissertation field note book, Erin Kane @Diana_monkey but not yet published.

Published data in McGraw et al., (2016) are from another study where the animals are not named.

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Anthropomorphic judgement values

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Anne being very involved with her cheetahs, although the paper (Hillborn et al., 2012) does not mention them by name.

 

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Another example of subjects with names Hubel et al., 2016), but this time named in the paper.

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Although in the description of methodology and results animals are referred to as subjects, the Table gives it away! (Allritz et al., 2016).

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Another example of named subjects (Stoinski et al., 2003).

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More named subjects (Dettmer & Fragaszy, 2000), but as these were captive the names almost certainly not chosen by the observers.

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In this case (Blake et al., 2016), use no human-based names either in the methods or tables, so exemplary, although of course I have not seen their field note books:-)

My concern, highlighted by these examples, is that by naming their study animals, the observers are anthropomorphising them and that this may lead them to inadvertently bias their observations. After all, the names have not been chosen at random, and thus could influence the behaviours noted (or ignored). I say ignored, because of two very specific examples, there are more, but I have these two to hand.

Victorians used birds as examples of good moral behaviour, erroneously believing them to be monogamous, probably because of seeing the way they fed their chicks cooperatively. Tim Birkhead (2000)* quotes the Reverend Frederick Morris who in 1853 preached  “Be thou like the dunnock – the male and female impeccably faithful to each other,”  and goes on to point out that despite a hundred years of ornithological science it was not until the late 1960s that  the promiscuous behaviour of female birds was revealed, interestingly enough coinciding with the new moral code of the 1960s.

Descriptions of penguin homosexual behaviour and their penchant for acts of necrophilia so shocked George Levick’s publishers that they removed them from his 1915 report but printed them and privately distributed them to selected parties marked as “Not for Publication” (Russell et al., 2012).  He also transcribed his descriptions of this ‘aberrant’ behaviour in Greek in his notebooks, presumably to make it less accessible.

And finally from me, this recent report about ‘sacred and ritualistic’ behaviour in chimpanzees Kuhl et al (2016),   where, I feel the authors have really allowed themselves to over-anthropomorphise with their subjects, very much to the detriment of scientific  detachment.  I have yet to find an entomologist who agrees with their interpretation. http://www.nature.com/articles/srep22219

AND NOW SOMETHING NEW for my blog, an embedded comment/riposte. I thought that it would be useful to get a response from someone who works on large charismatic mega-fauna and who names their subjects.  Anne Hilborn, whom many of you will know from Twitter as @AnneWHilborn, has kindly agreed to reply to my comments.  In the spirit of revealing any possible conflicts of interest I should say that I taught Anne when she was an Ecology MSc student at Silwood Park:-)

Over to you Anne…..

“Hello, my name is Anne and I name my study animals.”

Decades ago this might have gotten me jeered out of science, the assumption being that by naming my study animals I was anthropomorphizing them and that any conclusions I drew about their behavior would be suspect. Thankfully we (at least those of us who have the privilege of working on megafauna) have moved on a bit in our thinking and our ways of doing science.

There are two parts to Simon’s concern about naming study animals. One is that naming leads to anthropomorphization, the second is that the anthropomorphizing leads to biased science. I would argue that the naming of study animals doesn’t necessarily increase anthropomorphism. On the Serengeti Cheetah Project we don’t name cheetahs until they are independent from their mother (due to a high mortality rate).  During my PhD fieldwork I spent a lot of time following a young male known as HON752MC (son of Strudel).  Several months after I started my work he was named Boke. My interest in his behavior, my chagrin at his failures and happiness when he had a full belly didn’t change when he was named. Many of us get emotionally attached on some level to our study animals, whether they have names or numbers.

An interesting thing to ponder is that if naming does lead to anthropomorphizing, does it only happen when human names are used? What human characteristics am I likely to attach to cheetahs named Peanut, Muscat, Strudel, Fusili, or Chickpea?

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As to whether anthropomorphism leads to biased science… it definitely can if, as Simon points out, certain behaviors are not recorded because they do not fit the image of the animal the researcher had in their head. I don’t have any data on this, but I suspect this is extremely rare now days. Almost all researchers have had extensive formal training and know the importance of standardized data collection. I study cheetah hunting behavior, and I record how long a cheetahs spends spend stalking, chasing, killing, and eating their prey. I record the number of animals in the herd they targeted, how many second the cheetah spends eating vs being vigilant, and at what time they leave the carcass. No matter my personal feelings or attachments to an individual cheetah, the same data gets recorded.

Research methods have advanced a lot in the past decades and we use standardized methodologies and statistics expressly to prevent bias in our results. Anthropomorphism is just one possible source of bias, others include wanting to prove a treasured hypothesis, the tendency to place plots in areas where you suspect you will get the best results, etc..

As Adriana Lowe (@adriana_lowe ) puts it “Basically, if you’ve got a good study design and do appropriate stats, you can romanticise the furry little buggers until the cows come home and it won’t have a massive effect on your work. Any over interpretation of results would get called out by reviewers when you try to publish anyway.”

Simon points out examples of people being shocked when birds didn’t follow the dictates of contemporary human morality. I would like to think that biologists no longer place human values on animals. I can admire hyenas because the females are bigger bodied and socially dominant to males, but that doesn’t mean I draw parallels or lessons from them to human society (not in the least because the females give birth through their elongated clitoris and the cubs practice siblicide). As scientists we are capable of compartmentalizing, of caring deeply for our subjects, of shedding a tear when Asti turns up with one cub when previously she had five, without that changing the way we record data. In our training as biologists, we are taught not impose our own feelings or values on our study animals. We may find infanticide in lions (Packer and Pusey 1983), extra pair copulations in birds and primates (Sheldon 1994, Reichard 1995), or siblicide in boobies (Anderson 1990) to be repugnant, but we record, analyze, and try to publish on the phenomenon all the same.

To go on the offensive, there are ways naming study animals actually improves data collection.

Again, Adriana Lowe “If you’re doing scan sampling for instance, so writing down all individuals in a certain area every 10 minutes or so, names help. At least for me, it’s harder to remember if someone is M1 or M2 than Janet or Bob, particularly if you have a big study troop/community. So it can improve the quality of the data collected if you’re less likely to make identification errors.”

Because of our own training and peer review, assigning emotions or speculating about the intent on animals rarely makes it into scientific papers. However the situation is very different for those of us who wish to present our results outside of the ivory tower. While fellow scientists might be willing to wade through dry descriptions about how M43 contact called 3 times in 4 minutes when he was no longer in visual contact with M44, the public is not. Effective science communication needs a story and an emotional hook to draw people in. It is much easier to do that when you tell a story about Bradley and Cooper and not M43 and M44.  I will admit this does get into grey areas with the type of language we use outside of scientific papers. I tell stories about the cheetahs in my blog posts and even assign emotions to individuals. But if I am answering questions from the media or the public, I am still very careful not to make any definitive claims about behavior that haven’t been backed up by statistical analysis.

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Here I use language and make assumption in tweets that I never would in a scientific paper.

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There are a lot of issues that negatively affect the objectivity of science ie. the majority of funding going to well established entrenched researchers, papers being reviewed primarily by people from the same school of thought, the increasing pressure to have flashy results that generate headlines, but naming of study animals is not high on the list.

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So now, over to you the readers, what do you think? Please comment and share your views or at the very least, please cast your vote.

VOTE NOW

 

 

References

Allritz, M., Call, J. & Borkenau, P. (2016) How chimpanzees (Pan troglodytes) perform in a modified emotional Stroop task. Animal Cognition, 19, 435-449.

Anderson, D. J. (1990) Evolution of obligate siblicide in Boobies. 1. A test of the insurance-egg hypothesis. American Naturalist, 135, 334–350.

Birkhead, T. (2000) Promiscuity: An Evolutionary History of Sperm Competition and Sexual Conflict. Faber, London.

Blake, J.G., Mosquera, D., Loiselle, B.A., Swing, K., Guerra, J. & Romo, D. (2016) Spatial and temporal activity patterns of ocelots Leopardus pardalis in lowland forest of eastern Ecuador.  Journal of Mammalogy, 97, 455-463.

Dettmer, E., and Fragaszy, D. 2000. Determining the value of social companionship to captive tufted capuchin monkeys (Cebus apella). Journal of Applied Animal Welfare Science, 3, 293-304

Fuller, R. J., Oliver, T. H. & Leather, S. R. (2008). Forest management effects on carabid beetle communities in coniferous and broadleaved forests: implications for conservation. Insect Conservation & Diversity 1, 242-252.

Hillborn, A., Pettorelli, N., Orme, C.D.L. & Durant, S.M. (2012) Stalk and chase: how hunt stages affect hunting success in Serengeti cheetah. Animal Behaviour, 84, 701-706

Hubel, T.Y., Myatt, J.P., Jordan, N.R., Dewhirst, O.P., McNutt, J.W. & Wilson, A.M. (2016) Energy cost and return for hunting in African wild dogs and cheetahs. Nature Communications, 7, 11034 DOI:doi:10.1038/ncomms11034

Kühl, H.S., Kalan, A.K., Arandjelovic, M., Aubert, F., D’Auvergne, L., Goedmakers, A., Jones, S., Kehoe, L., Regnaut, S., Tickle, A., Ton, E., van Schijndel, J., Abwe, E.E., Angedakin, S., Agbor, A., Ayimisin, E.A., Bailey, E., Bessone, M., Bonnet, M., Brazolla, G., Buh, V.E., Chancellor, R., Cipoletta, C., Cohen, H., Corogenes, K., Coupland, C., Curran, B., Deschner, T., Dierks, K., Dieguez, P., Dilambaka, E., Diotoh, O., Dowd, D., Dunn, A., Eshuis, H., Fernandez, R., Ginath, Y., Hart, J., Hedwig, D., Ter Heegde, M., Hicks, T.C., Imong, I., Jeffery, K.J., Junker, J., Kadam, P., Kambi, M., Kienast, I., Kujirakwinja, D., Langergraber, K., Lapeyre, V., Lapuente, J., Lee, K., Leinert, V., Meier, A., Maretti, G., Marrocoli, S., Mbi, T.J., Mihindou, V., Moebius, Y., Morgan, D., Morgan, B., Mulindahabi, F., Murai, M., Niyigabae, P., Normand, E., Ntare, N., Ormsby, L.J., Piel, A., Pruetz, J., Rundus, A., Sanz, C., Sommer, V., Stewart, F., Tagg, N., Vanleeuwe, H., Vergnes, V., Willie, J., Wittig, R.M., Zuberbuehler, K., & Boesch, C. Chimpanzee accumulative stone throwing. Scientific Reports, 6, 22219.

Leather, S. R. (2009). Taxonomic chauvinism threatens the future of entomology. Biologist, 56, 10-13.

McGraw, W.S., van Casteren, A., Kane, E., Geissler, E., Burrows, B. & Dsaegling, D.J. (2016) Feeding and oral processing behaviors of two colobine monkeys in Tai Forest, Ivory Coast.  Journal of Human Evolution, in press.

Missa, O., Basset, Y., Alonso, A., Miller, S.E., Curletti, G., M., D.M., Eardley, C., Mansell, M.W., & Wagner, T. (2009) Monitoring arthropods in a tropical landscape: relative effects of sampling methods and habitat types on trap catches. Journal of Insect Conservation, 13, 103-118.

Packer, C. & Pusey, A.E. (1983) Adaptations of female lions to infanticide by incoming males. American Naturalist, 121, 716–728.

Ramsden, M.W., Menéndez, R., Leather, S.R., & Wakkers, 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.

Reichard, U. (1995) Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology ,100, 99–112.

Russell, D.G.D., Sladen, W.J.L. & Ainley, D.G. (2012) Dr. George Murray Levick (1876-1956): unpublished notes on the sexual habits of the Adélie penguin.  Polar Record, 48, 387-393

Sheldon, B. C. (1994) Male phenotype, fertility, and the pursuit of extra pair copulations by female birds. Proceedings of the Royal Society B: Biological Sciences, 257, 25–30.

Stoinski, T.S., Hoff, M.P. & Maple, T.L. (2003) Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition. American Journal of Primatology, 61, 61-72.

 

Post script

I said that entomologists don’t name their study animals but they do name their pets. Some of our PhD students had an African flower

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Soulcleaver; despite his name he seems quite cute when viewed side-on, perhaps even with a cheeky grin, although as an entomologist I couldn’t possibly say that:-)

beetle, Mecynorhina ugandiensis, which they named Soulcleaver, and I know that some beekeepers name their Queens https://missapismellifera.com/2016/03/17/the-decay-of-spring/

 

*note that Tim Birkhead also falls into the very trap that he describes by using the word promiscuous in the title of his book, a human judgemental term relating to moral behaviour, multiple mating would have been more appropriate.

 

 

 

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It’s never too early to get it right – children’s books can be accurate as well as fun

Making insects more appealing to children, (and adults), by making them look cute, cuddly and more like humans, is not a bad thing in itself, there is however, a line that should not be crossed.

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These two books for children written almost a century apart, are exact opposites. In Sibylle von Olfers’ Etwas von den Wurzelkindern published in 1906, we see the most incredibly detailed and accurate biological drawings.  The insects are pretty much recognizable to

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The Wurzelkindern getting the beetles spruced up for spring

species as are the flowering plants; the grasses are so accurately portrayed that the following conversation occurred on Twitter.

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Two plant scientists are able to discuss the grasses, so accurately are they drawn.

Contrast this with Birgitta Nicolas’ 2009 Der kleine Marienkäfer und seine Freunde.

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Here the insects have four legs*, humanised faces and hands and feet, although to be fair, the bumblebee does have pollen collectors (or is perhaps wearing leg warmers). The plants are heavily stylised and although one can guess at their families, I could not for example decide if the member of the Rosaceae pictured was Prunus, Malus or Pyrus, although being pink. it is most likely meant to be a Prunus.  The language used, despite the Gothic characters in von Olfer’s book, is at the same level, so meant to be read aloud by a parent or puzzled through by a beginner, yet the treatment of the wildlife is so different.  Von Olfers’ charming and accurate illustrations provide a visual treat of exploration and learning, while Nicolas’ heavily stylised daubs rely on the texturing present, i.e. fake fur for the squirrel, fuzzy felt for the bumble bee etc.  What harm would it have done to have at least given the insects the right number of legs and in the right place, all on the thorax.  The bee might also have liked to have had the right number of wings**, I might then have been able to forgive her the humanised faces, it is a story after all:-)

As Aristotle said “Give me a child until he is seven and I will show you the man.” Early habits die hard and if you learn that insects have four legs as a young child, confusion must ensue and make it harder to learn and retain the truth later on. First perceptions and impressions have a habit of sticking with us in later life, best to get the facts right at the beginning.

So if looking for an insect or natural history themed book for a young relative, I would recommend that you buy Sibylle von Olfer’s book and if your German or Google Translate is not up the job, you can get it in English https://www.amazon.co.uk/Tale-Root-Children-Etwas-Wurzelkindern/dp/3946190146/ref=sr_1_7?ie=UTF8&qid=1462291724&sr=8-7&keywords=etwas+von+den+wurzelkindern

Post script

Whilst clearing the attic in our new house*** in the Languedoc area of France, I came across this edition of Pinocchio published in 1959,

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which as well as bringing back nostalgic memories, I had the same edition as a child, but in English, is a great example of getting the insects right. The keen-eyed of you will notice it has a cricket on the front cover, but unlike the Walt Disney version in which Jiminy is definitely not a cricket, Libico Maraja, the illustrator, had obviously looked at crickets closely and carefully before putting pen to paper.

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Pinocchio meets the talking cricket – he does not have a name in the original version of the story.

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Even when anthropomorphised he still retains essential features such as legs joined to the thorax and complete with tarsi.

*although if you look closely, this insect, which I think is meant to be an aphid, does seem to have six legs:-)

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**at least the ladybird has elytra and wings 

***our retirement dream house and where I hope to write all the books that I have planned to write over the last twenty-odd years and never got round to doing 

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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 20th 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 Fig 1

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 Fig 2

 

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).

Berlese Fig 3

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.

Berlese Fig 4

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.

Berlese Fig 5

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.

Berlese Fig 6

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.

Berlese Fig 7

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

Berlese Fig 8

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.

Berlese Fig 9

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.

Berlese Fig 10

 

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

Berlese Fig 11

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

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

 

 

 

*a joint effort by me and Google Translate 

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EntoSci16 – a conference for future and budding entomologists

Fig 1a

Some of you may be wondering how this World’s first came about. Well, it was all due to Twitter. After a lot of nagging encouragement from one of my PhD students, I finally joined Twitter at the back-end of 2012. Shortly afterwards I met another new Tweeter, @Minibeastmayhem (Sally-Ann Spence in real life) who approached me with an idea that she had tried to get off the ground for a several years – an entomology conference for children. This sounded like a great idea to me and I was extremely surprised to hear that she had been told by various entomologists that it wouldn’t work. After a bit of ‘to and fro’ on Twitter we met up for a very nice Sunday lunch and hammered out a basic plan of action and a mission statement.

Fig 1b

Sally-Ann had done a lot of the preliminary work in approaching potential presenters and over the next couple of months we came up with a few more. I then sounded out my University (Harper Adams) who were very keen on the idea and agreed to do the publicity and the catering. We then began approaching a number of organisations for financial support and/or for stuff to put in the conference goodie bags. Surprisingly, some organisations that claim to support invertebrates and are keen on education, such as the RSPB and London Zoo, judging by their response, obviously didn’t even read our letters or only pay lip-service to the majority of the animal kingdom as they were singularly unhelpful.  Undeterred by these setbacks, we persevered, and with very generous support from the Royal Entomological Society , both financial and in the person of their Director of Outreach, Luke Tilley, were able to put together a very exciting package of events and presenters. And very importantly, because of the generosity of our sponsors, all free for the delegates. The big day, April 13th 2016, arrived and we were as ready as we would ever be. Almost 300 students and their accompanying adults (science teachers, careers teachers and some parents) turned up on the day, and to think that at one stage we were worried that no-one would be interested:-)

The delegates were all issued with colour-coded conference lanyards, and with the enthusiastic help of MSc and BSc students acting as guides, were then 

Fig 1

 

started on the action-packed, and hopefully enthralling and stimulating conference circuit.

Fig 2

George McGavin (our Patron) and Erica McAlister from the Natural History Museum (London) got the conference off to a great start with two very entertaining plenary talks about the wonders of entomology and flies respectively. After that it was on to the zones.

Graham & Janice Smith with the help of Tim Cockerill, were kept very busy with their Bugs and Beetles room, Steffan Gates (the Gastronaut) gave a dazzling and interactive display of entomophagy, Amoret Whitaker from the University of Winchester introduced the students to forensic entomology which included them processing a ‘maggot-infested crime scene’, and current and past MSc Entomology students (Soap Box Scientists), the Field Studies Council, RHS Wisley, and other exhibitors provided a very interactive and informative session in Zone 5. In the main lecture theatre, Max Barclay, Erica McAlister, George McGavin, Andy Salisbury, Darren Mann and Richard Comont were subjected to a barrage of questions ranging from how much they earned, to their favourite insects, their most dangerous insect encounter, some much easier to answer than others.

The day was especially long for some of us, as BBC Breakfast came and did some live filming, which meant that the organisers,  presenters and some hastily drafted in students had to put in an appearance at 0645. I think that they felt it was worth the effort though, if only to be able to say that they had been on TV.   All in all, the day was a real buzz. Of course the real stars were the insects and other invertebrates which managed to generate real enthusiasm among the delegates and their accompanying teachers. It was wonderful to see how many of the students responded so favourably to the insects, many of whom, at first, were reluctant to get close-up and personal with them. Seeing so many young people “oohing and aahing” rather than” yukking and gagging” really made my day. I really, truly believe, that we will be seeing many of the delegates becoming professional entomologists.

I leave you with a few images to give you the flavour of the day. For more professional images this link should keep you happy.

Fig 3

Early morning preparation, coffee was very much needed

Fig 4

And we’re off to a great start

Fig 5

and it just kept getting better

Fig 6

and better

Fig 7

Some of the team, Luke Tilley, Sally-Ann Spence, Graham Smith, Tim Cockerill, George McGavin and me.

 

Fig 8

A really huge thank you to Laura Coulthard and Helen Foster, from the Harper Adams Marketing and Communications Department, who put their hearts and souls into making sure that the event ran smoothly. We couldn’t have done it without them.

And who knows, perhaps we will do it all again next year:-)

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