Small and frequently overlooked, but without them we could not exist

Without them, we would find the world a very different place, that is if we were still alive.  Yet very few people give them a thought, and then usually only to dismiss them or castigate them for impinging on our comfortable lives. Animals without backbones, the micro-flora and fauna, are what keep the world a place in which we can make a living.  Politicians however, and many others of our fellow travellers on this fragile planet, seem unaware of their importance.  Donald Trump rescinds environmental protection laws as if they are a hindrance to humankind rather than a boon, BREXIT politicians and their supporters in the UK extol the virtues of escaping from those silly EU environmental laws that prevent them from polluting our beaches and rivers and making our air unbreathable. We all need to take a step back and adjust our vision so that we can appreciate the little things that run the world and understand that despite our size, our abundance and our apparent dominance, that we too are a part of nature.

I and many others have written about this topic on many occasions but it is a message that bears repetition again and again.  I leave you with the passage that stimulated my latest rant and a few links to similar pieces.

“In terms of size, mammals are an anomaly, as the vast majority of the world’s existing animal species are snail-sized or smaller.  It’s almost as if, regardless of your kingdom, the smaller your size and the earlier your place on the tree of life, the more critical is your niche on Earth; snails and worms create soil, and blue-green algae create oxygen; mammals seem comparatively dispensable; the result of the random path of evolution over a luxurious amount of time.”

Elizabeth Tova Bailey  (2010)  – The Sound of a Wild Snail Eating

Here are a few links to give you food for thought and to inspire you to find more of the same.

Michael Samways  Small animals rule the world. We need to stop destroying them

E O Wilson (1987) The little things that rule the world

Gregory Mueller & John Schmidt (2007) on why we should know more about fungi

Robert May (2009) Ecological science and tomorrow’s world

Mark Gessner and colleagues (2010) on the importance of decomposers

Anders Dahlberg and colleagues (2010) on why we should conserve fungi

Anne Maczulak (2010) on the importance of bacteria

Me complaining about plastic and other environmental dangers

Me again, this time about conserving small things

Sorry, but me again, this time about appreciating nature

and from Gerald Durrell, who was a great inspiration to me through his various writings…

And finally, If you haven’t read this, then I can certainly recommend it:

Ehrlich, P.  & Ehrlich, A. (1981) Extinction, Random House, New York.

 

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Pick and mix – eclectic links to stuff that caught my interest last week

Hopefully some of these links may be of interest to some of you.

 

Scientists, admittedly probably not all, can appreciate and enjoy poetry, as Stephen Heard points out here

On the Death’s Head Hawkmoth as a honey thief

For those of you who like France, bees and might be considering becoming beekeepers

On the value of native trees and shrubs for wildlife

On a similar vein, here is a paper about the value of native trees for insectivorous birds

More evidence of the importance of biodiversity for ecosystem functioning

The Journal of Biogeography celebrates the 50th anniversary of the publication of The Theory of Island biogeography by posing fifty fundamental questions that might take the discipline further forward

Another one from one of my favourite French sites, this time on the beauties of mosses and lichens

A French farmer asks for help from politicians using an ingenious message board

Over on Dynamic Ecology Jeremy Fox asks if you can think of any successful ecological models based on loose physical analogies?

And finally, announcing the launch of Pantheon, the tool to help you analyse your invertebrate species samples

 

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Sloth Moths – moving faster than their hosts

One of the minor downsides of our Biology and Taxonomy of Insects module on the MSc course is, that we do have to review a lot of families within some of the groups, Lepidoptera being a prime example.  Current estimates range from 250 000 to 500 000 species in 124 families (Kristensen et al., 2007). Going through the basic biology of each family can be pretty dry stuff, even if I have a personal anecdote or two to help lighten information overload.  I am, for example, able to wax lyrical for several minutes about small ermine moths and their incredible silk-production activities, but even after more than 40 years of playing around with insects I don’t have a personal story for every family of Lepidoptera 🙂 so I am always on the lookout for an extra interesting or mind-blowing fact to help leaven the student’s knowledge diet.

Imagine my delight then when I came across a clip* from a BBC One Wildlife programme, Ingenious Animals, describing an obligate association between sloths and moths and not just because of the rhyming opportunity** 🙂

Sloth with moths – BBC One Ingenious Animals

The earliest record of a moth associated with a sloth that I have been able to find is in 1877 (Westwood, 1877) which merely records that the unidentified moth was “parasitic on the three-toed sloth”. In 1908 a Mr August Busck on a visit to Panama saw a two-toed sloth, Choloepus hoffmanni fall from a tree and noticed several moths flying out of the sloth’s fur.  He caught these and on his return to the United States presented them to Dr Harrison Dyar (Dyar, 1908a).  If the name seems familiar to you that is because Harrison Dyar is better known in connection with Dyar’s Law, the observation that larval growth in arthropods is predictable and follows a geometric progression (Dyar, 1890). The moths were identified by Dyar as a new species which he named Cryptoses choloepi.  Dyar hypothesised that the moths and their larvae lived in the fur of the sloth and it was this that caused the sloth’s matted hair.

Cryptoses choloepi (Lepidoptera, Chrysauginae)

http://nmnh.typepad.com/department_of_entomology/2014/03/sloths-moths-and-algae-whos-eating-whom.html

Shortly after publishing the first note Dyar came across two more moth specimens, this time collected from a sloth in Costa Rica.  He felt that these were another species, possibly Bradipodicola hahneli (Dyar, 1908b).  The next mention of a sloth moth that I could fine is in a marvellously titled paper (Tate, 1931) who refers to a moth shot in western Ecuador whose fur was “literally alive with a small species of moth, whose larvae possibly fed on the greenish algae which grew in the hair”.  The idea that sloth moths fed on the fur of living sloths was further reinforced by Brues (1936) although this was not based on any personal observations.  It was only in 1976 that it was discovered that the larvae of the sloth moth Cryptoses choloepi were actually coprophagous (Waage & Montgomery, 1976), the female moths waiting for the three-toes sloth B. infuscatus to descend from the trees to relive their bowels, which they do about once a week.  As an aside, I have known Jeff Waage for many years in his role as a biological control expert but until I discovered this paper about a month ago, had no idea that he had ever spent time inspecting sloth faeces 🙂  Jeff and his co-author Gene Montgomery, described the association between the moths and the sloths as phoretic, rather than parasitic, as they saw no harm being caused to the sloths, but a number of benefits accruing to the moths, namely oviposition-site location being simplified, the fur of the sloth acting as refuge from avian predators and diet enhancement from sloth secretions (Waage, 1980).  It turns out however, that some species of sloth moth do spend their whole life cycle on the sloth, B. hahneli lose their wings once a sloth host is found and their eggs are laid in the fur of the sloth (Greenfield, 1981).  The algae that these moths presumably feed on is considered to be in a symbiotic association with the sloths, providing camouflage and possibly nutrition in the form of trace elements (Gilmore et al., 2001).  Hereby lies a tale.  The two-toed sloths have a much wider diet and home range than three-toed sloths and also defecate from the trees, unlike the three-toed sloths which have a very narrow diet (entirely leaves) and narrow home ranges, yet descend from the relative safety of the forest canopy to defecate, albeit only once a week, but still a risky undertaking (Pauli et al., 2017).  Rather than a phoretic relationship Pauli and colleagues see the relationship between sloths, algae and moths as a three-way mutualism, beautifully summarised in their Figure 3.

Postulated linked mutualisms (þ) among sloths, moths and algae: (a) sloths descend their tree to defecate, and deliver gravid female sloth moths (þ) to oviposition sites in their dung; (b) larval moths are copraphagous and as adults seek sloths in the canopy; (c) moths represent portals for nutrients, and via decomposition and mineralization by detritivores increase inorganic nitrogen levels in sloth fur, which fuels algal (þ) growth, and (d ) sloths (þ) then consume these algae-gardens, presumably to augment their limited diet. This figure brazenly ‘borrowed’ from Pauli et al. 2014).

The sloths take the risk of increased predation by descending to ground level, because by helping the moths they improve their own nutrition and hence their fitness.  Yet another great example of the wonders of the natural world.

 

Post script

Although not as exotic as the sloth moth, we in the UK can also lay claim to a coprophagous moth, Aglossa pinguinalis, the Large Tabby which feeds on, among other things, sheep dung.  In Spain it is recorded as a cave dweller feeding almost entirely on animal dung, apparently not being too fussy as to the source.

 

References

Bradley, J.D. (1982) Two new species of moths (Lepidoptera, Pyralidae, Chrysauginae) associated with the three-toed sloth (Bradypus spp.) in South America.  Acta Amazonica, 12, 649-656.

Brues, C.T. (1936) Aberrant feeding behaviour among insects and its bearing on the development of specialized food habits.  Quarterly Review of Biology, 11, 305-319.

Dyar, H.G. (1890) The number of molts of lepidopterous larvae. Psyche, 5, 420–422.

Dyar, H.G. (1908a) A pyralid inhabiting the fur of the living sloth.  Proceedings of the Entomological Society of Washington, 9, 169-170.

Dyar, H.H. (1908b) A further note on the sloth moth. Proceedings of the Entomological Society of Washington, 10, 81-82.

Dyar, H.G. (1912) More about the sloth moth. Proceedings of the Entomological Society of Washington, 14, 142-144.

Gilmore, D.PP., Da Costa, C.P. & Duarte, D.P.F. (2001) Sloth biology: an update on their physiological ecology, behaviour and role as vectors of arthropods and arboviruses.  Brazilian Journal of Medical and Biological Research, 34, 9-25.

Greenfield, M.D. (1981) Moth sex pheromones: an evolutionary perspective.  The Florida Entomologist, 64, 4-17.

Kristensen, N., Scoble, M.J. & Karsholt, O. (2007)  Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity.  Zootaxa, 1668, 699-747.

Pauli, J.N., Mendoza, J.E., Steffan, S.A., Carey, C.C., Weimer, P.J. & Peery, M.Z. (2014) A syndrome of mutualism reinfocrs the lifestyle of a sloth.  Proceedings of the Royal Society B, 281, 20133006. http://dx.doi.org/10.1098/rspb.2013.3006.

Pinero, F.S. & Lopez, F.J.P. (1998) Coprophagy in Lepidoptera: observational and experimental evidence in the pyralid moth Aglossa pinguinalisJournal of Zoology London, 244, 357-362.

Tate, G.H.H. (1931) Random observations on habits of South American mammals.  Journal of Mammalogy, 12, 248-256.

Waage, J.K. (1980) Sloth moths and other zoophilous Lepidoptera.  Proceedings of the British Entomological and Natural History Society, 13, 73-74.

Waage, J.K. & Montgomery, G.G. (1976) Crytopses choloepi: a coprophagous moth that lives on a sloth.  Science, 193, 157-158.

Westwood, J.O. (1877) XXVIII. Entomological Notes.  Transactions of the Entomological Society, 25, 431-439.

 

*For the clip about the sloth moth see here http://www.bbc.co.uk/programmes/p04840xn

**Now, when I see a sloth,

My first thought is for the moth,

That has to make that desperate jump

When the sloth decides to take a dump!

 

 

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Ladybird, ladybug or Alder warbler

Insects with common names are usually those that are notable in some way, be that because they are causing us harm or are beautiful, brightly coloured and give us joy.  Vernacular names for agricultural pest insects usually refer to the crop they are harming, such as the grain aphid, the apple moth, the large pine weevil.  For non-pests however, names appear more arbitrary.  One of the most well-known and loved insect, is the ladybird, or if you are from North America, the ladybug.  These are not, however, the only names that these useful animals have acquired since they first attracted human attention.  They have, over the centuries, acquired a wonderful variety of names around the world.o start with, you may well ask why they have the prefix lady.  In England they were originally called “Our Lady’s bird”.  Leaving aside the mystery of why they were called birds, the first part of the name referred to the fact that the most commonly noticed ladybirds are red (albeit with white or black spots), and in the Middle ages images of the Virgin Mary usually showed her in a red dress.  Another linkage to the Virgin Mary is that the most commonly seen ladybird is the seven spot ladybird (Coccinella septempunctata), and this was associated with the Seven Joys and the Seven Sorrows of Mary.

 

The association with Mary is also seen in Spanish, mariquita, meaning little Mary and in German Marienkäfer, Mary’s beetle.  The reference to the colour red is reflected in the fact that ladybirds belong to the family Coccinellidae which comes from the Latin for scarlet, coccineus, see also cochineal.

Other languages also make reference to the Virgin Mary, in Bosnian, as in German, they are called Mary’s beetle, bubamara.  The Basuques, as far as I can make out with the help of Google Translate, refer to them as Mary’s yolk, marigorringoa. The religious association is also seen in Dutch, lieveheersbeestje which means  the Lord’s sweet little creature.  The Russians call ladybirds Божья коровка [bozhya korovka] which translates to God’s little cow. Lithuanians have two names for ladybirds, Dievo karvytė  God’s cow  but also call them boružė .  The Welsh have lost the religious reference and instead refer to ladybirds as red cows, buwch goch gota. The Greeks make a religious link with a reference to Easter, pashalitsa (Easter is Pasha), but also refer to it as “kind of beetle with fine plumage (feathers)”, είδος κάνθαρου με ωραία πτερά.  The Portuguese have opted for joaninha (ninha means baby), whereas the Slovenians and Slovaks have homed in on the spots, ladybird being pikapolonica (pika is dot) and slunéčko sedmitečné  (sedmit is seven) respectively. The Bulgarians call them калинка (kalinka) but the Finns take the prize for the most obscure name, with Leppäkerttu, which literally translated means alder warbler 🙂

It seems apposite, that as in Finnish they apparently sing,  I should include these two rhymes; one that most of us have come across in some form or other

 

and one from Sweden that will probably be less familiar to English speakers, but which similarly exhorts the ladybird to fly away and at the same time introduces yet another feathered name for the ladybird.

Guld-höna, guld-ko!
Flyg öster, flyg vester,
Dit du flyger der bor din älskade!

Gold-hen, gold-cow!
Fly east, fly west,
You’ll fly to where your sweetheart lives.

 

A gold cow with wings – Kamadhenu  a wish-fulfilling Hindu goddess

In Hindi, ladybirds are called sonapankhi, or golden wings and are associated with passing or failing exams, depending on whether it stays on your hand long enough for you to count the spots or not.

And finally, to prove that not all verse about ladybirds is doggerel, this poem by the poet Clive Sansom captures both the beauty and fragility of nature.

The Ladybird

Tiniest of turtles!
Your shining back
Is a shell of orange
With spots of black.

How trustingly you walk
Across this land
Of hairgrass and hollows
That is my hand.

Your small wire legs,
So frail, so thin,
Their touch is swansdown
Upon my skin.

There! break out
Your wings and fly:
No tenderer creature
Beneath the sky.

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Have you read The Origin of the Species?

As biologists we all acknowledge the influence that Charles Darwin has had on our professional lives but how many of us have actually read On the Origin of Species by Means of Natural Selection in its entirety?  The importance of The Origin has long been recognised by universities, even we agricultural zoology students at Leeds University back in 1973 had The Origin on our first year recommended reading list.  How many of my classmates bought it, let alone actually read it, is anyone’s guess.  I suspect not many.  I was somewhat odd, in that I had already read it, as far as I can remember when I was about 16 and just starting in the Lower 6th  (Year 12 in today’s parlance).  I was helped by the fact that both my parents were biologists and my Dad’s copy of The Origin was readily available. I was, and still am, a prodigious reader, although I must confess that I now find it much more difficult to read ‘hard’ books than I did then.

Finally, here is my question.  If as a professional biologist, of whatever ilk, does not having read The Origin make you any less of a biologist?  Should you be outed and castigated as an incomplete biologist?  Probably not.  What do you think?  I asked how many people had read  The Origin using a Twitter survey last week as a simple yes/no question.  The survey generated 53 responses, of  which 57% said yes.  The survey below is slightly more nuanced, taking into account the one respondent who tweeted “partially?”  🙂 Just realised that I managed to miss out the less than 18 category, my apologies.  If you are such a prodigy please feel free to tick the 18-25 box but add a note in the comments section so that I can adjust later.

 

Many thanks for your participation and rest assured, if you have not read The Origin I am not judging you in any way  🙂

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The Verrall Supper 2017 – entomologists eating, drinking and getting very merry

The Rembrandt Hotel in South Kensington and the first Wednesday of March mean only one thing to many UK entomologists – the Verrall Supper. I have written about the Verrall Supper previously on more than one occasion, so this will, once again, be largely a photographic record.  This year the first Wednesday of March was March 1st and this seemed to have caught a few Verrallers by surprise.  Consequently, numbers were slightly down compared with last year’s record, but the number of non-attending Verrallers paying to retain their membership was at an all-time high.  One notable absence was the former Verrall Secretary, Helmut van Emden who due to mobility problems was unable to attend, only the second one that he has missed in 50 years!

On a very sad note, we reported the deaths of two long-time members of the Association, Gerry Tremewan (long time editor of The Entomologist and the Entomologist’s Gazette, and Bernard Skinner, author of that magnificent book,  Moths of the British Isles.

More positively, we were slightly up on female entomologist this year, 30% compared with last year’s 29%.  There is still much progress to be made, but we have seen a year on year increase now for the last four years so, perhaps one day we will hit that magic 50:50 mark.

Our entomologist in Holy Orders, the Reverend Dr David Agassiz, was unable to attend this year, so instead of the usual entomological grace, I performed a humanist blessing, which seemed to meet with satisfaction from all sides.  I reproduce it here if anyone feels like using it at a similar occasion.

As we come together at this special time, let us pause a moment to appreciate the opportunity for good company and to thank all those past and present whose efforts have made this event possible. As we go through life, the most important thing that we can collect is good memories.  Thank you for all being here today to share this meal as a treasured part of this collection.

And now to let the pictures tell the story.

Chris Lyal and Clive Farrell of the Entomological Club – “helping” at the registration desk

Three very illustrious (or should that be shiny) entomologists – Jeremy Thomas, Charles Godfray and Dick Vane-Wright

Richard Harrington and the winner of the Van Emden Bursary, PhD student Ellen Moss

Two of the more venerable Verrallers – Trevor Lewis and Marion Gratwick

Many Verrallers are young and quite a few are female 🙂

Adriana De Palma making a fuss about Erica McAlister’s new book 🙂

Some older entomologists enjoying the food and drink

The younger entomologists also had excellent appetites

The President of the Royal Entomological Society, Mike Hassell, wishes you all good health and happiness

Beards still feature among the younger end of the male Verrallers, although sadly it is no longer mandatory 🙂

And a bit of entomological bling to bring the show to an end 🙂

Many thanks to all who attended and I hope to see you all again next year, plus many new faces.

 

 

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Will Lucretia Cutter reign supreme? Beetle Queen – the latest sensation from M G Leonard

beetle-queen

https://www.chickenhousebooks.com/books/beetle-queen/

Laughter, tears, joy, horror and shock; what an emotional roller-coaster of a book.  From the gurgling stomach of a much-loved uncle to the charred rim of a once beetle-inhabited cup, Maya Leonard’s latest installment* of beetle-inspired fiction will grip and hold you spell-bound from the moment you start reading.  This is a book you won’t be able to put down, it will get in the way of everyday life, and will, depending on when you begin to read it, obscure your dinner plate or breakfast bowl.  Be warned, those of you who are moved to tears easily will definitely need a box of tissues or a large handkerchief close by.

It is very hard to write a review of this enthralling and fast-moving book without giving away too many spoilers, so I am going to limit myself to unstinting praise and a very brief synopsis of the plot to give you a flavour of what to expect 🙂

Metamorphosis is the name of the game. Lucretia Cutter has a devious plan, but Darkus, Bertolt and Virginia are on the case. Novak thinks that Darkus is dead, Bartholomew Cuttle is acting very strangely, Uncle Max is a tower of strength and Mrs Bloom reveals hidden depths. We learn more about the early days of Darkus’s parents and their interactions with the then Lucy Johnstone and meet some other entomologists.  Yellow ladybirds act as spies and assassins for Lucretia Cutter, and we travel to the film Awards in Los Angeles via Greenland with our resourceful trio, Uncle Max and Mrs Bloom.  Lurking in the background, the evil cousins Humphrey and Pickering provide comic, albeit distasteful relief.  All this leads us to the dramatic finale, where much is revealed including some parts which will especially amuse all the boys (old and young) 🙂

The shootout at the Film Awards ceremony where the evil Lucretia spectacularly reveals her hidden attributes, Novak performs gravity-defying feats, and giant motorised pooters come into their own to help our intrepid trio and their grown-up allies overcome the evil hordes, makes me think that one day we will be seeing Darkus and his friends on the silver screen.  There are of course great supporting roles by Baxter, Marvin, Newton and Hepburn, and do remember to brush up on your Morse code 🙂

This installment of the story ends at Christmas and the presents our heroes receive tell us that our next stop is the Amazon!

This book, like the first will definitely help bring the wonders of entomology to a wider audience.  Maya Leonard continues to be a worthy ambassador for our discipline, and I am extremely grateful that she has opted to use her undoubted talents to publicise insects and entomology so well.  Thank you Maya.

ento16-fantastic-finish

*If you haven’t read the first installment in this thrilling trilogy I can thoroughly recommend it.

 

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An inordinate fondness for biodiversity – a visit behind the scenes at the Natural History Museum

Last week  (13th February) I traveled with the MSc Entomology students to the Natural History Museum, London.  As part of their course they are taken behind the scenes and meet some of the curators and their favourite beasts.  This one of my favourite course trips and although I have made the pilgrimage for many years I always find something new to marvel at as well as reacquainting myself with some of my old favourites.  After an early start (0645) we arrived exactly on time (for a change), 10.30, at the Museum site in South Kensington.  I always have mixed feelings about South Kensington, having spent twenty years of my life commuting to Imperial College, just up the road from the museum.  I loved teaching on the Applied Ecology course I ran, but over the years the working atmosphere in the Department became really toxic* and I was extremely glad to move to my present location, Harper Adams University.  After signing in, which with twenty students took some time, Erica McAlister (@flygirl) led us through the thronged galleries (it was half term) to the staff

nhm1

Nostalgia time, my first biological memory, aged 3.

areas, where the research, identification and curating takes place.  Our first port of call was the Diptera where Erica regaled us with lurid tales of flies, big and small, beneficial and pestiferous.

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Erica McAlister extolling the virtues of bot flies

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Any one fancy cake for tea?  Kungu cake, made from African gnats

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Early advisory poster

As we left to move on to the Hymenopteran, hosted by David Notton, I noticed this classic poster warning against mosquitoes.  David chose bees as the main focus of his part of the tour, which as four of the students will be doing bee-based research projects was very apt.

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Admiring the bees

Whilst the students were engrossed with the bees I did a bit of fossicking and was amused to find that tobacco boxes were obviously a preferred choice by Scandinavian Hymenopterists in which to send their specimens to the museum.

nhm-tobacco

Finnish and Swedish tobacco boxes being put to good use

Next was that most eminent of Coleopterists, Max @Coleopterist Barclay who as usual enthralled the students and me, with stories of

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Max Barclay demonstrating a Lindgren funnel and talking about ‘fossilised’ dung balls

beetles large and small, anecdotes of Darwin and Wallace and the amusing story of how ancient clay-encased dung balls were for many years thought by anthropologists and archaeologists to be remnants of early humankind’s bolas hunting equipment.  It was only when someone accidentally broke one and found a long-dead dung beetle inside that the truth was revealed 🙂

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Often overlooked, the Natural History Museum is an exhibit in itself

 As we were leaving to move on to the Lepidoptera section, I felt obliged to point out to the students that not only is the outside of the museum stunningly beautiful but that the interior is also a work of art in itself, something that a lot of visitors tend to overlook. Once in the Lepidoptera section  Geoff Martin proudly displayed his magnificent collection of Lepidoptera, gaudy and otherwise, including the type specimen of the Queen Alexandra’s Birdwing which was captured with the aid of a shotgun!

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Lepidopterist, Geoff Martin, vying with his subjects in colourful appearance 🙂

Lunch and a chance to enjoy the galleries was next on the agenda.  Unfortunately, as it was half term this was easier said than done, although I did find a sunny spot to eat my packed lunch, as a Yorkshireman I always find the prices charged for refreshments by museums somewhat a painful.  In an almost deserted gallery I came across this rather nice picture.

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A lovely piece of historical entomological art.

Then it was on to the Spirit Collection.  Erica had laid on a special treat, Oliver Crimmen, fish man extraordinaire.  I may be an entomologist but I can sympathise with this branch of vertebrate zoology.  Fish, like insects are undeservedly ranked below the furries, despite being the most speciose vertebrate group.  I have been in the Spirit Room many times but have never seen inside the giant metal tanks.  Some of these, as Ollie demonstrated with a refreshing disregard for health and safety, are filled with giant fish floating in 70% alcohol.

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Fish man, Oliver Crimmen, literally getting to grips with his subjects.

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A fantastic end to the day culminated with a group photo with a spectacular set of choppers 🙂

Many thanks to Erica McAlister for hosting and organising our visit and to the NHM staff who passionately attempted to convert the students to their respective ‘pets’.

*one day I will write about it.

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EntoMasters on Tour – Visit to the Royal Entomological Society 2017

Yesterday I accompanied the Harper Adams University MSc Entomology and Integrated Pest Management students on their annual visit to the Headquarters of the Royal Entomological Society (RES), The Mansion House, located on the outskirts of the historic city of St Albans.

ontour-1

Harper Adams University entomologists, young and not so young 🙂  Photo by Jhman Kundun

Last year we had  a truly epic journey; accidents on the overcrowded UK motorway system on the way there and back, meant that we spent eight hours on the coach 😦  This year, in trying to avoid a similar fate, I cruelly forced the students and staff to be on the coach by 0645.

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Early morning entomologists; despite the hour, happy and smiling  – photo Alex Dye

Unfortunately, despite the early start, a diesel spill closed the M6 at a crucial moment causing huge queues and long detours.  As a result we arrived at our destination a frustratingly  hour and a half late.  Entomologists are however, made of stern stuff and the coffee and delicious biscuits awaiting our arrival soon restored our spirits.

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Coffee!

After coffee the RES Director of Science, Professor Jim Hardie, welcomed the students and talked about the history of the society and the benefits of joining as student members.  This was followed by a brief talk by one of the Outreach Team, Francisca Sconce, herself a former entomology Master’s student, about the many ways in which the RES brings the study and appreciation of insects to a wider audience.  The students were then treated to lunch and given the opportunity to explore the building and its facilities and to look at some of the treasures that the RES safeguards for posterity.

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Someone found the aphid section 🙂

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A future President? – trying out the presidential chair for size

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Dr Andy Cherrill enjoying the famous entomological lift (elevator)

I am no stranger to The Mansion House; I have taken several cohorts of the entomology MSc students to the Royal Entomological Society since the society moved its headquarters to St Albans in 2007, and also visit the building a couple of times a year when attending committee meetings.  Despite my long association with the RES (40 years) I still however, find things I have never seen before, such as the print below, that gently pokes fun at the single-mindedness of the entomological specialist.

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It is only a vertebrate  🙂

I also never cease to be amazed and humbled by the history that surrounds one as you meander your way around the various library rooms.

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Printed history – as beautiful today as it was 400 years ago

We had a wonderful and educational day and you will be pleased to hear that our return journey was trouble-free.  Finally, many thanks to the Royal Entomological Society and staff for their extremely kind hospitality; the lunch was, as always, filling and delicious  🙂

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Not all aphids are farmed by ants

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Aren’t insects wonderful?

 

References

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

*in my opinion at any rate 🙂

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

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

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

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

 

Post script

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

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

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Filed under Aphidology, Aphids