Category Archives: Science writing

Red, green or gold? Autumn colours and aphid host choice

“The falling leaves
Drift by my window
The falling leaves
Of red and gold”

red-green-or-gold-1

Red, green and gold, all on one tree

When Frank Sinatra sang Autumn Leaves he was almost certainly not thinking of aphids and I am pretty certain that the English lyricist, Johnny Mercer, who translated the words from the original French by Jacques Prévert wasn’t either 🙂

The colours we see in autumn are mainly due to two classes of pigment, the carotenoids (yellow-orange; think carrot) and the anthocyanins (red-purple).  Carotenoids are present in the leaves all year round but are masked by the green chlorophyll.  Chlorophyll breaks down in autumn, leaving the yellow carotenes visible.  The anthocyanins on the other hand are not formed until autumn (Sanger, 1971; Lee & Gould, 2002) and this mixture of pigments give us the colours that have inspired so many artists.

red-green-or-gold-2

Autumn Leaves Georgia O’Keeffe (1924) Tate Modern

To many, autumn starts with the appearance of the first turning leaves, to me it is the arrival of gynoparae* of the bird cherry-oat aphid (Rhopalosiphum padi) on my bird cherry (Prunus padus) trees.

red-green-or-gold-3

Bird cherry, Prunus padus, leaves on the turn.

Little did I know when I started my PhD in 1977 that almost thirty years later I would be part of a raging debate about the function of autumn colouration in woody plants. At the time I was interested in the colonisation patterns (or as I pretentiously termed it in my thesis ‘remigration’) of bird cherry aphids from their secondary grass and cereal host plants to their primary host bird cherry.  My study system was 30 bird cherry saplings divided between two cold frames in the Biology Compound at the University of East Anglia (Norwich).  Every day from the middle of August until leaf fall I checked every leaf of each tree, for gynoparae, males and oviparae, carefully noting the position of each leaf, its phenological stage and giving it a unique number. I repeated this in the autumns of 1978 and 1979.  The phenological stage was based on the leaf colour: green, mature; yellow, mature to senescent; red, senescent.  What I reported was that more gynoparae landed on green and yellow leaves than on red and that the gynoparae on green and yellow leaves survived for longer and produced more offspring (oviparae), than those on red leaves (Leather, 1981).   The gynoparae of the bird cherry aphid are quite special in that although as adults they do not feed (Leather, 1982), they do not land on bird cherry trees at random (Leather & Lehti, 1982), but choose trees that not only do their offspring (the oviparae) do better on, but that also favour those aphids hatching from eggs in the spring (Leather, 1986).  It should not have come as a surprise then, that when I analysed some of the data I had collected all those years ago, their preference for green and yellow leaves over red ones, is linked to how long those

red-green-or-gold-4

Figure 1. Length of time leaves remained on tree after first colonisation by gynoparae of Rhopalosiphum padi (F = 30.1 df 2/77, P <0.001)

leaves have left to live (Figure 1). The timing of events at this time of year, has, of necessity, got to be very precise. The egg-laying females (oviparae) are unable to develop on mature bird cherry leaves (Leather & Dixon, 1981), but it seems that the bird cherry aphid has this under control, making its decisions about the timing of the production of autumn forms (morphs) sometime in August (Ward et al., 1984).  All very sensible as far as I was concerned and that was as far as I took things.  Subsequent work by Furuta (1986) supported this in that he showed that maple aphids settled on and reproduced on green-yellow and yellow-orange leaves but avoided red leaves which had shorter life spans.

Jump forward fifteen years or so, and in a paper, that at the time, had somehow passed me by, the late great Bill Hamilton and Sam Brown (Hamilton & Brown, 2001) hypothesised that trees with an intense autumn display, similarly to those brightly coloured animals that signal their distastefulness with yellows, blacks and reds, were signalling their unsuitability as a host plant to aphids.  Like the costs imposed on insects that sequester plant toxins to protect themselves against predators, the production of anthocyanins responsible for the red autumn colouration is expensive, especially when you consider that the leaves have only a short time left to live (Hoch et al., 2001).  In autumn, trees and woody shrubs are normally mobilising resources in the leaves and moving them back into themselves ready to be used again the following spring (Dixon, 1963). Ecologists and evolutionary biologists were thus keen to explain the phenomenon in terms of trade-offs, for example, fruit flags that advertise the position of fruits for those trees that rely on seed dispersal by vertebrates (Stiles, 1982) or as ultra-violet screens to prevent tissue damage (Merzlyak & Gittelson, 1995).  Hamilton & Brown felt that these hypotheses were either, in the case of the fruit flag, only applicable to trees with fruit present and, in the latter, untenable. Instead they advocated the ‘signalling hypothesis’ which was based on the premise that trees that suffer from a lot of aphids (attacked by more than one species rather than by large numbers of a single species), invest in greater levels of defence and in autumn advertise this using bright warning colours.   The premise being, that although it is metabolically expensive for the plants to produce these colours, it is worth the investment if they result in a reduction in aphid attack.

This hypothesis was not without its detractors. Others suggested, that far from avoiding red colours, aphids were attracted to yellow or green as an indicator of host nutrition (Wilkinson et al., (2002).  Holopainen & Peltonen (2002) also suggested that birch aphids use the onset of autumn colours to pick out those trees where nutrient retranslocation was happening, and thus with higher levels of soluble nitrogen in the leaves.  This was of course, what I was trying to confirm back when I was doing my PhD.  Conversely, supporters of the signalling hypothesis, argued that trees (birch again) that could ‘afford’ to produce bright autumn colours were fitter, so more resistant in general and that they were warning potential herbivores of this by a bright autumn display (Hagen et al 2004).

Round about this time (2002), I was approached by a young Swiss researcher, Marco Archetti, who knew that I had a plot of sixty bird cherry trees that I had planted up when I arrived at Silwood in 1992, originally designed to follow-up some work that I had begun whilst at the Forestry Commission looking at the effects of early season defoliation on subsequent tree growth (Leather, 1993, 1995).  Marco convinced me that I had the ideal set-up to test the ‘signalling hypothesis’ and what was to be a very fruitful collaboration began.

We counted arriving gynoparae and their offspring (oviparae) throughout October (Marco making trips over from Oxford where he was then based**) noting leaf colour before and after each count.  As with my PhD work we found that the greener trees were preferentially colonised by the gynoparae and that more oviparae were produced on those trees and that given what I had found earlier that bird cherry aphid gynoparae chose trees that are good hosts in spring (Leather, 1986), Marco felt that we were able to support the honest signalling hypothesis (Archetti & Leather, 2005).  I was slightly less comfortable about this, as there are only two species of aphid that attack bird cherry and one of those is very rare and the original signalling hypothesis was based on the premise that it was trees that were attacked by a lot of aphid species that used the red colouration as a keep clear signal.  Anyway, it was published 🙂

That said, others agreed with us, for example, Schaefer & Rolshausen (2006) who called it the defence indication hypothesis, arguing that bright colours advertise high levels of plant defence and that the herbivores would do well to stay away from those plants displaying them. On the other hand, Sinkkonen (2006) suggested that reproductively active plants produce autumn colours early to deter insects from feeding on them and thus reduce their seed set.

Chittka & Döring (2007) on the other hand, suggested that there is no need to look further than yellow carotenoids acting as integral components of photosynthesis and protection against light damage and red anthocyanins preventing photo-inhibition (Hoch et al., 2001) as to why trees turn colourful in autumn.  In other words, nothing to do with the insects at all.  A couple of years later however, Thomas Döring and Marco got together with another former colleague of mine from Silwood Park, Jim Hardie, and changed their minds slightly.  This time, whilst conceding that red leaves are not attractive to aphids but noting that yellow leaves are even more attractive than green ones, suggested that the red colour could be being used to mask yellow (Döring et al., 2009).

Others have their own pet theories.  In recent years, veteran Australian entomologist Tom White has become interested in the concept of insect species that specifically feed on senescent plant tissue (White, 2002, 2015) and added to the debate by suggesting that aphids in general are senescence feeders and thus choose green and yellow as they have longest time to live and that the red leaves are also nitrogen depleted (White, 2009) which is supported by my PhD data (Figure 1).  This resulted in a spirited response by Lev-Yadun & Holopainen (2011) who claimed that he had misunderstood the scenario in thinking that leaves go sequentially from green to yellow to red, which they suggest is rare (I question this) and that actually in trees that go from green to red, the leaves still contain significant amounts of nitrogen, so a deterrent signal is still required.

red-green-or-gold-5

Maple, green to yellow in this case

red-green-or-gold-6

Spindle, Euonymus europaeus, green to red

What about those trees and other plants that have red or purple leaves in the spring or all year round and not just in autumn?

red-green-or-gold-7

Some trees have red foliage all year

Trees like some of the ornamental cherries or copper beech? I haven’t been able to find any papers that suggest that red or purple-leaved varieties of beech and cherries are less susceptible to aphid attack.  My own observations, probably imperfectly recalled, are that copper beech is regularly infested by the beech woolly aphid, Phyllaphis fagi , and just as heavily, if not more so than the normal green-leaved  beech trees.  That of course may just be a reflection that the white waxy wool covering the aphid stands out more against the red leaves.  Perhaps someone out here might like to check this out?  Some work that my friend and former colleague, Allan Watt, (sadly unpublished) did many years ago in Scotland looking at the effect of beech species and cultivar on infestation levels by the beech leaf mining weevil, Rhynchaenus fagi, did not indicate any differences between copper and green cultivars.  It does seem however, that in cabbages, leaf colour can tell the specialist cabbage aphid, Brevicoryne brassciae, if plants are well defended or not, the bluer the cabbage, the nastier it is (Green et al, 2015).

To summarise:

  1. Red leaves are produced by the trees in autumn to reduce ultraviolet damage and protect metabolic processes in the leaf.
  2. Red leaves are deliberately produced by the tree to warn aphids that their leaves are well defended – honest signalling.
  3. Red leaves are produced by the tree to ‘fool’ the herbivores that the leaves are likely to drop soon and warn them to keep away so as to safeguard their fruit – dishonest signalling.
  4. The tree is blissfully unaware of the aphids and the aphids are exploiting the intensity of the autumn colours produced by the trees to select which are the best trees to colonise in terms of nutrition and length of time left on the tree.

As I write, the debate still goes on and we seem no nearer to arriving at a definitive answer to the riddle of why trees produce bright leaves in autumn.  If nothing else however, the debate has generated a lot of interest and enabled people to sneak some amusing titles into the scientific literature.  Do make the effort to read the titles of some of the references below.

References

Archetti, M. (2009) Phylogenetic analysis reveals a scattered distribution of autumn colours. Annals of Botany, 103, 703-713.

Archetti, M. & Leather, S.R. (2005) A test of the coevolution theory of autumn colours: colour preference of Rhopalosiphum padi on Prunus padus.  Oikos, 110, 339-343.

Chittka, L. & Döring, T.F. (2007) Are autumn foliage colors red signals to aphids? PLoS Biology , 5(8): e187. Doi:10.1371/journal.pbio.0050187.

Dixon, A.F.G. (1963) Reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr) (Hemiptera, Aphididae). Journal of Animal Ecology, 32, 33-48.

Döring, T.F., Archetti, M. & Hardie, J. (2009) Autumn leaves seen through herbivore eyes.  Proceedings of the Royal Society London B., 276, 121-127.

Furuta, K. (1986) Host preferences and population dynamics in an autumnal population of the maple aphid, Periphyllus californiensis Shinji (Homoptera: Aphididae). Zeitschrift fur Angewandte Entomologie, 102, 93-100.

Green, J.P., Foster, R., Wilkins, L., Osorio, D. & Hartley, S.E. (2015) Leaf colour as a signal of chemical defence to insect herbivores in wild cabbage (Brassica oleracea).  PLoS ONE, 10(9): e0136884.doi:10.1371/journal.pone.0136884.

Hagen, S.B. (2004) Autumn coloration as a signal of tree condition. Proceedings of the Royal Society London B, 271, S184-S185.

Hamilton, W.D. & Brown, S.P. (2001) Autumn tree colours as handicap signal. Proceedings of the Royal Society London B, 268, 1489-1493.

Hoch , W.A.,  Zeldin, E.L. & McCown, B.H. (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiology, 21, 1-8.

Holopainen, J.K. & Peltonen, P. (2002) Bright colours of deciduous trees attract aphids: nutrient retranslocation hypothesis.  Oikos, 99, 184-188.

Leather, S.R. (1981) Reproduction and survival: a field study of the gynoparae of the bird cherry-oat aphid, Rhopalosiphum padi (L.). Annales Entomologici Fennici, 47, 131-135.

Leather, S.R. (1982) Do gynoparae and males need to feed? An attempt to allocate resources in the bird cherry-oat aphid Rhopalosiphum padiEntomologia experimentalis et applicata, 31, 386-390.

Leather, S.R. (1986) Host monitoring by aphid migrants: do gynoparae maximise offspring fitness? Oecologia, 68, 367-369.

Leather, S.R. (1993) Early season defoliation of bird cherry influences autumn colonization by the bird cherry aphid, Rhopalosiphum padi. Oikos, 66, 43-47.

Leather, S.R. (1995) Medium term effects of early season defoliation on the colonisation of bird cherry (Prunus padus L.). European Journal of Entomology, 92, 623-631.

Leather, S.R. & Dixon, A.F.G. (1981) Growth, survival and reproduction of the bird-cherry aphid, Rhopalosiphum padi, on its primary host. Annals of Applied Biology, 99, 115-118.

Leather, S.R. & Lehti, J.P. (1982) Field studies on the factors affecting the population dynamics of the bird cherry-oat aphid, Rhopalosiphum padi (L.) in Finland. Annales Agriculturae Fenniae, 21, 20-31.

Lee, D.W. & Gould, K.S. (2002) Anthocyanins in leaves and other vegetative organs: An introduction. Advances in Botanical Research, 37, 1-16.

Lev-Yadun, S. & Holopainen, J.K. (2011) How red is the red autumn leaf herring and did it lose its red color? Plant Signalling & Behavior, 6, 1879-1880.

Merzlyak, W.N. & Gittelson, A. (1995) Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescing leaves (Acer platanoides L.). Journal of Plant Physiology, 145, 315-320.

Sanger, J.E. (1971) Quantitative investigations of leaf pigments from their Inception in buds through autumn coloration to decomposition in falling leaves.  Ecology, 52, 1075-1089.

Schaefer, H.M. & Rolshausen, G. (2006) Plants on red alert – do insects pay attentionBioEssays, 28, 65-71.

Sinkkonen, A. (2006) Do autumn leaf colours serve as reproductive insurance against sucking herbivores?  Oikos, 113, 557-562.

Stiles, E.W. (1982) Fruit flags: two hypotheses. American Naturalist, 120, 500-509.

Ward, S.A., Leather, S.R., & Dixon, A.F.G. (1984) Temperature prediction and the timing of sex in aphids. Oecologia, 62, 230-233.

White, T.C.R. (2003) Nutrient translocation hypothesis: a subsect of the flush-feeding/senescence-feeding hypothesis. Oikos, 103, 217.

White, T.C.R. (2009) Catching a red herring: autumn colours and aphids. Oikos, 118, 1610-1612.

White, T.C.R. (2015) Senescence-feesders: a new trophic subguild of insect herbivore. Journal of Applied Entomology, 139, 11-22.

Wilkinson, D.M., Sherratt, T.N., Phillip, D.M., Wratten, S.D., Dixon, A.F.G. & Young, A.J. (2002) The adaptive significance of autumn colours.  Oikos, 99, 402-407.

 

 *for a detailed account of the wonderful terminology associated with aphid life cycles read here

**coincidentally he is now a Lecturer at the University of East Anglia in the same Department where I did my PhD

8 Comments

Filed under Aphidology, Aphids, Science writing

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.

 

7 Comments

Filed under EntoNotes, Science writing

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.

OB1

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.

OB2

Anthropomorphic judgement values

OB3

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

 

OB4

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

OB5

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

OB6

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

OB7

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

OB8

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?

OB9

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.

OB10

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

OB11

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.

——————————————————————————————————————–

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

OB12

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.

 

 

 

12 Comments

Filed under Bugbears, Science writing, Uncategorized

When frustration becomes serendipitous – My second most cited paper

For most of the 1980s and the early 1990s I worked for the UK Forestry Commission as a research and advisory entomologist. As a civil servant I was subjected to a lot more rules than I am now as a university academic. The most frustrating set of rules in my mind, were those associated with publishing papers. The initial consultation with a statistician before your experiment was planned and any subsequent collaboration with the analysis was very sensible, and I had no problems with that part of the process at all. Our statisticians were very good in that they helped you decide the analysis but expected you to learn GenStat (the Forestry Commission standard statistics programme) and do it yourself unless you were really stuck.

The next bit was the frustrating part. When it came to writing papers you first submitted your paper to your line manager. They then read your paper, very frustrating indeed for me, as my immediate boss considered papers a very low priority and it could be several months before he got around to passing it back with comments and suggestions. Then it was passed to a member of one of the other department such as silviculture, tree breeding or pathology for them to read and make comments. The idea behind this being that it helped make the paper accessible to a wide audience, again a good idea. The problem at this stage was that once again your paper was likely to be a low priority, so yet more delay. Once that was done you then had to submit your paper to the Chief Research Office for him to read and comment on, so once again yet more delay. This meant that quite often it was a year before you actually were able to submit your paper to a journal, which could be deeply frustrating to say the least.

Frustrated

In 1986 a new journal to be published by the British Ecological Society was announced, Functional Ecology. In those days, the dreaded Impact Factors had not yet raised their ugly heads, and one tended to publish in journals relevant to your discipline, or, as in this case, the fancy took you.  I thought it would be cool to publish in the first issue of the first volume of this new journal.  I therefore set to work, with the help of one of our statisticians to produce a paper about life history parameters of the pine beauty moth, from a more ecological point of view and not from the more applied view-point of it as a forest pest (my job remit). I was very proud of the paper and confess to having got somewhat carried away in the discussion, so much so, that it was suggested by all who read it in the very lengthy internal appraisal process, that most of the discussion should be cut as being too far away from the main story. As the process had taken so long already I decided to go with the flow and eventually submitted my paper about a year after first writing it, incidentally giving my statistician a co-authorship. It was accepted and did indeed appear in the first volume of Functional Ecology, albeit the last of the year (Leather & Burnand, 1987)! It has to date (14th October 2015) being cited 53 times, by no means a disgrace, but certainly not my second-most cited paper.

I mentioned earlier that I was really proud of my discussion and I decided that I was going to publish it regardless. I reworked it slightly and submitted it to Oikos as a Forum piece, taking the calculated risk of not submitting it through the official Forestry Commission system. My reasoning was, that a), it was unlikely to be read by anyone in the Forestry Commission, being a very ecological journal, and b), if challenged I would say that it had already been seen by the powers that be, albeit not officially. To my relief it was accepted as is (Leather, 1988) and my immediate boss never mentioned it. To my surprise and delight this is now my second-most cited paper, having so far acquired 207 citations and still picks up a reasonable number of cites every year. I guess that I should actually be grateful to all those internal referees who insisted that I cut my discussion down so drastically.

References

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

Leather, S.R. & Burnand, A.C. (1987) Factors affecting life-history parameters of the pine beauty moth, Panolis flammea (D&S): the hidden costs of reproduction. Functional Ecology, 1, 331-338.

 

Post script

In case you wondered, my most cited paper is an Annual Review paper, written with one of my former PhD students, Caroline Awmack, and now has almost a thousand citations (994 as of today).

Reference

Awmack, C. S. &Leather, S. R. (2002). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817-844.

 

4 Comments

Filed under Bugbears, Science writing, Uncategorized

Journals of Irreproducible Research – downgrading reproducibility and fact checking

As far as I am concerned, good science is about communication and reproducibility, or, as Stephen Heard argues, at least being able to believe that it is reproducible.  I would argue a bit more strongly than Stephen, in that I think you should, at the very least, be able to be confident that you could reproduce the experiment without having to contact the author(s) and that you can also easily check the cited literature.   In this context, there are two things that really annoy me about some of the so-called ’high impact’ established print journals and their on-line would be rivals.  First, the way in which the methods and materials section is relegated to the end of the paper, often in smaller font, and in some cases to the supplementary material section  In other journals e.g. Nature, the methods section is also very minimal and I defy anyone to repeat those experiments!  My second bugbear is the habit that some journals have, possibly to reduce space, in making you use numbers to denote references, placing them either in parentheses or superscript in the main text.

Perhaps I am alone in this, but I do like to know whose work is being cited without having to constantly refer to the references section.  What  particularly annoys me, are those journals that not only insist on numbered references but then list them in number order and not in alphabetical order!  I once wrote a review paper for Annual Review of Entomology, which has the numbering system, but subverted it by listing my references alphabetically – the editor never noticed 😉

You may say that what all these journals are doing is merely structuring the paper in the order that people tend to read them which is, I admit, a valid point. To me however, they are saying to the scientific community, perhaps not overtly, but certainly subliminally, that methods and materials are something you don’t really need to bother about, somewhat akin to those things that you store in an attic or basement, just in case you might want them at some time in the future, but probably not often, if at all.

Hidden methods

This sends a strong and erroneous message to authors that despite the methodology being the most important part of how we do our science, as long as they report the general gist of how they did things it is fine.  To referees the subversion of the methods section sends an equally strong signal; you don’t really need to spend a lot of time reading about the methodology as long as the rationale for the work is justified and that the results are significant and well presented.

As someone who works on insect-plant interactions I constantly come across inadequate methods and materials sections both as a referee and as a reader of published work.  The thing that perhaps causes me the most annoyance are descriptions of plant phenology.   Herbivorous insects have a very intimate relationship with their host plants and the growth stage of their host plant or the age of the plant tissue that they are feeding on can have very marked effects on their development, survival and fecundity (Awmack & Leather, 2002).  I so often came across methods descriptions along the lines of “10 day-old cabbage seedling” “ 3 week old pepper plant”,  “2 week-old wheat plant”, that in desperation I wrote an editorial (Leather, 2010) explaining how important it was to use a measure that didn’t depend on the temperature,  photoperiod, nutrient or water status that the plants were grown at i.e. the BCCH scale.  I also compiled a virtual issue of Annals of Applied Biology, with relevant examples drawn from the journal which has a long and distinguished history in publishing such articles.  If you can’t find your host plant in past issues of the Annals you will find that most plants have a published version somewhere, even if only on Wikipedia.  Despite my efforts however, I still often have to remind authors to describe the phenological stage of their host plants accurately and precisely.

Methods and materials, please come back, we need you!

 

References

Awmack, C. S. & Leather, S. R. (2002). Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817-844.

Leather, S. R. (2010). Precise knowledge of plant growth stages enhances applied and pure research. Annals of Applied Biology 157, 159-161.

 

7 Comments

Filed under Bugbears, Science writing, Uncategorized