Scorpion flies – not as scary as they sound or look

I’m very fond of Scorpionflies, in fact, they are almost up there with aphids on my all-time favourite insects list. They, at least to me, are reminiscent of something that one would expect to find in Lewis Carrol’s Alice in Wonderland. They belong to the Order Mecoptera, which until some pesky taxonomists decided that fleas are Mecoptera, was one of the smaller insect Orders with just 600 species, if fleas are indeed Mecoptera then we now have 2600!

Male (left) and female (right) Scorpion flies. Despite the resemblance to the back end of a scorpion it is not a sting, but part of the male genitalia.

Ignoring fleas for the moment, there are nine families of Mecoptera, but only three are common; Scorpion flies (Panorpidae), the Hanging flies (Bittacidae) and Snow fleas (Boreidae) (Byers & Thornhill, 1983). Of these only two occur in the UK, the Scorpion flies and the Snow fleas. Adult Scorpion flies are mostly scavengers, mainly eating dead insects, topping this up with a bit of pollen, nectar and fruit juice and for a special treat, bird faeces. Their larvae live in the soil and mop up whatever dead things they come across.

The Snow fleas feed on moss and are only getting a mention here because they are quite cute and for a few years I held the record for the furthest north record 😊

Cute Snow fleas 😊

The Hanging flies are carnivores capturing live prey as adults and larvae and deserve a special mention as they (and although it shouldn’t, but it appeals to the ten-year old in me, makes me giggle) have a penisfilum.

Male (left) and female of Bittacus planus. Photo provided by Dr. Baozhen Hua. Note the knob in the male!

Anyway, back to the scorpion flies. They are found in temperate regions, worldwide and as of 2018 there were 280 species. The males are highly competitive, as are many of the Mecoptera. Males will fight over their food, which as I mentioned earlier is quite high in dead flies, which they often steal from spider webs.  They have no fear of spiders as they can dissolve the web if they do get caught.

Another cool thing about scorpion flies is that they, like some spiders, use nuptial gifts to increase their chance of mating. They first use a pheromone which as pheromones go, is pretty short range, 10 -15 metres. Once a female has been enticed by the pheromone, the males than flash their wings, which are striped and do a bit of a dance. Depending on species, what happens next could be one of three tactics.

Nuptial gifts and mating of Dicerapanorpa magna Photo provided by Dr. Baozhen Hua.

male gives female food which she eats during copulation either a salivary deposit from enlarged salivary glands or a dead insect, and waits female arrival.  Another tactic is to find a suitable dead insect which he then stands by, waits for a female to arrive, and then copulates with her while she eats it. Some males are less generous and will force themselves on a female without any presents or even pheromones, holding their chosen mate in place with his abdominal clamp (Tong et al., 2018). The size of the gift is related to the duration of copulation and to how long it will be before the female mates with a different male (Byers & Thornhill, 1983); females that were subjected to forced copulation have a very short inhibition time – the more the males invest in their nuptial gifts, the more offspring they sire. Basically, they get what they pay for! The eggs, usually no more than ten per clutch, are laid into damp soil.

When I introduce Scorpionflies to a new audience, I am, as I find frequently with other insects, faced with the usual human exceptionalism question “

“Mecoptera are most often defined by the characters they do not possess” Penny (2016)

They are not pollinators generally regarded as pollinators (thanks Jeff Ollerton for reminding me that some do visit flowers for nectar), but they are not crop pests and nor are they vectors. We don’t eat them and most of them most are not biological control agents. Bittacids are, however, predators. Panorpids are recyclers, they feed on carrion. The Nannochoristids could be seen as s bio-indicators; their larvae need clean water and Boreids could act as climate change ‘canaries’ because of their limited dispersal ability and their need for cold.

Scorpionflies have appeared in video games (Shelomi, 2019) so I guess are helping the economy and keeping people entertained.

In the long distance past (170 MYA), before angiosperms made their appearance and allowed the explosion in insect diversity possible, three groups of scorpionfly, now extinct, fed on the nectar of gymnosperms and in return pollinated them (Ren et al., 2009).

References

Byers, G.W. & Thornhill, R. (1983) Biology of the Mecoptera. Annual Review of Entomology, 28, 203-228.

Palmer, C. (2010) Diversity of feeding strategies in adult Mecoptera. Terrestrial Arthropod Reviews, 3, 111-128.

Ren, D., Labandeira, C.C., et al., (2009) A probable pollination mode before angiosperms: Eurasian long-proboscid scorpionflies. Science, 326, 840-847.

Shelomi, M. (2019). Entomoludology: Arthropods in Video Games. American Entomologist, 65, 97–106

Tong, X., Zhong, W. & Hua, B.Z. (2018) Copulatory mechanism and functional morphology of genitalia and anal horn of the scorpionfly Cerapanorpa dubia (Mecoptera: Panorpidae). Journal of Morphology, 279, 1532-1539.

Citizen Science Rules – The ‘humble’ amateur is the backbone of entomology – laud them, don’t scorn them

I know we deal with invertebrates but the exoskeleton of entomology doesn’t quite hack it 😊 There is a tendency within academia, perhaps not as marked as it was when I entered it, to be somewhat dismissive, even scornful, when it comes to natural historians and amateurs. I once had a bit of an in-print argument with the late Denis Owen about the validity of data collected by ‘amateurs’ (Leather, 1990), which I found a bit surprising considering his wife Jennifer’s deep and life-long involvement with that type of data (Owen, 2010).

I have been a ‘professional’ entomologist for more than forty years and although I may, in the past, when I was imbued with the arrogance of youth, have made remarks about stamp collecting and lack of scientific method, I have always been in awe of the taxonomic expert, whom at a glance can accurately (most of the time) identify an insect to species. Me, I’m pleased when I get the family right.  I remember when I was an undergraduate sitting round a light trap on our field course, being stunned by Judy Honecker (where are you now?) shouting out the names of the moths as they flew into it – all done by the mysterious jizz. She may of course, have been taking advantage of our ignorance, but I don’t think so.

I don’t think, even now, that many academic, research-active, professional entomologists, or ecologists really appreciate the service that the amateur entomologist or in a broader sense, natural historian, provides to the professional community.  I am a long-time member of the British Entomological and Natural History Society (BENHS) which means that a copy of the British Journal of Entomology and Natural History pops through my letter box every three months. Every time I open a copy of this little journal I am humbled by

Latest issue of the British Journal of Entomology and Natural History

the erudition displayed by the contents.  You won’t find professionally crafted accounts of large-scale field studies/experiment or complex laboratory experiments, analysed using the most complicated analysis that packages such as R or SPSS can spit out by any means.  What you will find, and this is perhaps where the slightly scornful attitude to the ‘amateur’ has its roots, are reports of insects found while on holiday in Spain or closer to home* and accounts of the annual exhibition. You will also find note of the first records of species in the UK, new host records, be they plants or other animals, and yes, also reports of experimental work.  The style may not be as ‘scientific’ as that found in mainstream scientific journals, but that does not detract from their value. The thing that really blows my mind about the BJENHS and others of its ilk such as the Entomologist’s Monthly Magazine, (in both of which I have published), are the numbers of new records reported and the identification skills that these demonstrate of the authors. It struck me that whereas those entomologists with similar skills that work within academia, either in museums or universities, are described as systematists (naturalists engaged in classification) or taxonomists (biologists that groups organisms into categories) these expert amateurs didn’t seem to have a single word to describe them. I of course resorted to Twitter to see if anyone out there knew better.

I received a number of responses, the one below summing up the most common answers.

Pretty much the status quo.

One person suggested parataxonomist, which I feel means an entirely different thing, being someone who has been trained to have “expertise is in collecting specimens, mounting them, and performing preliminary sorting of the specimens to morphospecies” (Basset et al., 2000).

What I do think we can all agree on, is that the county recorders, the various group specialists and more general natural historians, are what I would term professional amateurs. They are not paid for what they do, most have jobs outside entomology, or are, in many cases, retired, but they approach their subject in a thoroughly professional way, keeping impeccable records and disseminating their findings through publications, talks at meetings and running (or helping run) training courses.  They do a huge service for entomology, not just by providing data for the ‘professionals’ to mine and analyse, but also by encouraging others to enter the field. The professional and the professional amateur can, sometimes exist in the same person, I was for example, once President of the Amateur Entomologist’s Society and the current President, Erica McAlister (@flygirlNHM, for those of you on Twitter), is also a professional entomologist.

Richard Jones rather neatly summing it all up.

There is now, however, a whole new category of amateur. Citizen science has unleashed the ‘amateur amateur’ into the wild, albeit many stray no further than their gardens. Citizen science, once a bit marginalised, is now pretty much mainstream is fully recognised by the professional ecologists and entomologists as a hugely important contribution to their disciplines Bates et al., 2013; Pernat et al., 2021). The two most publicised UK examples are the Big Butterfly Count (incidentally this year’s launch coinciding with the publication of this post) and the Big Garden Birdwatch, both of which my wife and I do. Despite having my name on ten papers dealing with birds, I count myself when it comes to the latter, as being a true ‘amateur amateur’ 😊

Citizen science projects span disciplines and the globe.  You can take part in a ‘bioblitz’, record the timing of budburst, the number of plants in flower on a particular date, join in the UK ladybird survey, see how many birds you can count over the Christmas period, and many, many others.

I think it is extremely important to take note of the quote below. It explains to some extent, why in the past, and sadly, to a certain extent, why some (not many thankfully) professional scientists still tend to treat citizen science with less respect than it deserves.

 “Traditionally, we think in terms of a data-gathering component of science, a data analysis component of science, and an interpretive “discussion” component of science. As well, the scientific method is typically thought of as being hypothesis driven (with the hypothesis or “question”preceding data collection), and in mainstream science the process of generating and testing hypotheses is the domain of the researchers – those people who are unequivocally “scientists”. In citizen science, the participants are almost exclusively involved in data gathering alone, but most projects include the promise that anyone is welcome to follow through with their own analyses and interpretations. This is the key element that makes citizen science “democratic”, even if a few participants follow up with analyses of their own. “Citizen Scientist” is, therefore, best understood as an honorary title, given to anyone who participates in any level of the scientific enterprise, on a voluntary basis, with the proviso that that most participants are involved only in data collection.” Acorn (2017)

The data that we collect as citizen scientists is not wasted, and compares well with the data collected by the professionals (Pocock et al., 2015; Pernat et al., 2021) and as the picture below illustrates, is of immense value to entomologists and ecologists.

Roger Morris at Dipterist’s Forum June 27^th 2021 ‘When I started it was as rare as rocking horse faeces’ – Roger Morris talking about recording Rhingia rostrata. Roger is highlighting why recording schemes are so useful. Picture from Twitter via @FlygirlNHM)

Just to reiterate the importance of these glorious amateurs.  Just as those insect host records collected and published by the professional amateurs enabled the late Sir Richard Southwood to restart the species-area concept (Southwood, 1961) and give many of us an opportunity to lengthen our publication lists, so today’s army of professional and amateur amateurs are providing data for a new generation of entomologists and ecologists to help understand and explain the changes we are seeing in insect abundance and distribution (e.g. Werenkraut et al., 2020).  It is very important that their contribution is neither overlooked nor unrecognised.  Without them we would be lost.

Did you know that the oldest (unless you know of an older one?) Citizen Science project in the world is the Christmas Bird Count in the USA, which was started in 1900?

References

Acorn, J. (2017). Entomological citizen science in Canada. The Canadian Entomologist, 149, 774-785.

Basset, Y., Novotny, V., Miller, S.E. & Pyle, R. (2000) Quantifying biodiversity: experience with parataxonomists and digital photography in Papua New Guinea and Guyana. BioScience, 50, 899-908.

Bates, A.J., Sadler, J.P., Everett, G., Grundy, D., Lowe, N., Davis, G., Baker, D., Bridge, M., Clifton, J., Freestone, R., Gardner, D., Gibson, C.W.D., Hemming, R., Howarth, S., Orridge, S., Shaw, M., Tams, T., & Young, H. (2013) Assessing the value of the Garden Moth Scheme citizen science dataset: how does light trap type affect catch? Entomologia experimentalis et applicata, 146, 386-397.

Leather, S.R. (1990) The analysis of species-area relationships, with particular reference to macrolepidoptera on Rosaceae: how important is insect data-set quality? The Entomologist, 109, 8-16.

Owen, J. (2010) Wildlife of a Garden; A Thirty-year Study, Royal Horticultural Society, London.

Pernat, N., Kampen, H., Jeschke, J.M. & Werner, D. (2021) Citizen science versus professional data collection: Comparison of approaches to mosquito monitoring in Germany. Journal of Applied Ecology, 58, 214-223.

Pocock, M.J.O., Roy, H.E., Preston, C.D., & Roy, D.B. (2015) The Biological Records Centre: a pioneer of citizen science. Biological Journal of the Linnaean Society, 115, 475-493.

Southwood, T.R.E. (1961) The number of species of insect associated with various trees. Journal of Animal Ecology, 30, 1-8.

Werenkraut, V., Baudino, F., & Roy, H.E. (2020) Citizen science reveals the distribution of the invasive harlequin ladybird (Harmonia axyridis Pallas) in Argentina. Biological Invasions, 22, 2915-2921.

*I remember reading with great amusement a short article in the Entomologist’s Monthly Magazine from the early part of the 20^th Century describing the ‘discovery’ of a species new to Britain that had flown into the bathroom of the author (a retired Lt. Colonel if I recall correctly) while he was having a bath.

Planes, trains and automobiles – insect killers?

I couldn’t not use this – it is (sadly) one of my favourite films 😊

Anyone who has driven (or walked) along a road will have come across roadkill, be it squirrels, pheasants, badgers, deer or even something more exotic, perhaps it us only us entomologists who notice the squashed invertebrates ☹

Dead carabids and mayflies Shay Lane, Staffordshire, 8^th June 2021

But, lets leave the roadkill for a moment, and in the spirit of the title of the film, start in the air. The first thing I discovered when I started to search for the effects of aircraft on insects is the paucity of literature on the subject – it turns out that people are much more interested in stopping disease carrying insects being transported by air or, and coming as a bit of a surprise to me, stopping insects causing plane crashes (House et al., 2020; Grout & Russell, 2021). The aircraft industry is so concerned about the physical dangers posed to ‘planes by insects that NASA actually have a Bug Team dedicated to developing insect proof aircraft.

I am, however, more concerned about how dangerous aircraft are to insects. First, we need to know how many insects are up there and what the probability of them being struck and killed by aircraft is. I’m guessing that bug strike is pretty common, otherwise NASA wouldn’t have a Bug Team. The majority of insects in the air are found at 300-600 m, although this does vary in relation to time of day (Reynolds et al., 2005). Getting a figure for the actual number of insects in the air is as you might expect, actually quite difficult.  The first attempt to trap and collect insects using an aircraft was in 1926 in Louisiana (USA) using a specially designed trap (Glick, 1939).  These do not seem to have been particularly effective as 5 years of trapping, involving 1528 hours of flying, caught just under 30 000 insects (Glick, 1939).  Those of us who have operated pitfall traps for any length of time would consider this a very modest haul 😊

Glick (1939) The aircraft insect trap

That said, the exercise was obviously more hazardous than even collecting insects from roundabouts as this very laconic extract highlights:

 “The skill of the pilots who flew the collecting airplanes is evidenced by the fact that no fatalities occurred.  Only one major accident occurred, when a forced landing resulted in the destruction of the craft and injury to both the pilot (McGinley) and the writer. Such mishaps must be expected in a more or less hazardous undertaking.”

The distribution of catch number was very similar to that reported from the more recent UK study using radar (Reynolds et al., 2005) and is reinforced by this statement from the NASA Bug Team; “The reason we do these tests at low altitudes or do a lot of takeoffs and landings is because bug accumulation occurs at anywhere from the ground to less than 1,000 feet,” said Mia Siochi, a materials researcher at NASA Langley”.

Given the number of flights made globally and the investment being made into protecting aircraft from bug strike, I would assume that the number of insects being killed by aircraft worldwide is probably very high. I am sure that someone with the skill, time and inclination, can probably come up with a fairly realistic figure.  Over to you Dear Readers.

Next up, if we keep to the film title, are trains.  There has been a bit more work looking at the damage that trains do to insects, not a lot, but something is better than nothing.  Work collecting train kill from railway lines showed that snails were particularly vulnerable to being run over, similar to the effects on trail-following ermine moth caterpillars that I observed in Finland in 1981, with Ephemeroptera (Mayflies) in second place (Pop et al., 2020). This, as the authors suggest, was almost certainly due to the time of year and the presence of a lake nearby. Unfortunately no one has done the equivalent of a train splatometer which might be rewarding as these observations from correspondence in British Birds magazine suggest that locomotive engines are causing some mortality to flying insects.  Over to you Bug Life. How about getting the train companies to fit splatometers?

Finally, cars and their effect on insect life. There is anecdotal evidence out there, after all as drivers we have all seen moths in our headlights at night and used our windscreen washers and wipers to try and remove dried on insect corpses and their haemolymph from our front windscreens.

An observation by Ian Bedford

My front bumper – sadly (or perhaps not) much less insect spattered than in the past

Yes, anecdotally we know that insects are being hit by cars (see above) and on my front number plate, a couple of weeks ago (beginning of June) I counted 73 insects, mainly aphids after a 245 km trip. The problem as I see it, is quantifying the numbers killed and calculating the effect that this has on insect abundance. I have mentioned the splatometer in an earlier post which attempts to standardise the number plate counts and I am pleased to see that this has now been revived by Bug Life, and will hopefully carry on for many years. The idea behind this is that over the years we will be able to see if insect numbers as reflected by the change in numbers of splats are increasing, decreasing of remaining the same.  This will not, certainly as described, tell us how many insects are being killed by road using vehicles, although it would be possible if the data were collected over delineated stretches of road (Baxter-Gilbert et al., 2015).  It is not just flying insects that are killed by cars; not all flying insects fly across roads, many seem happy to walk to the other side, reckless as that may seem.

A brave, or possibly fool-hardy carabid beetle crossing the road – Guild Lane, Sutton, Staffordshire, 9^th June 2021.

There have been enough studies done looking at the interactions between roads and insects for a review article to have been published fairly recently, although not all the papers deal directly with mortality effects (Munõz et al., 2015). Many studies have recorded the species affected and the number of dead individuals found but few have attempted to calculate what this means in total. Most studies, as we might expect, have been on large, easily identifiable charismatic species (Munõz et al., 2015) and it from these that we do have some idea of the magnitude of the mayhem caused by road traffic. Some of the figures are incredibly high. A survey of Odonata road kill, albeit near a wetland, of two 500 m stretches of dual carriageway in the Great Lakes region of the USA revealed that at least 88/km/day were being hit and killed by vehicles (Riffell, 1969).  Another study in the USA, this time on Lepidoptera, calculated that about 20 000 000 butterflies (mainly Pieridae) were killed in one week in September (McKenna et al., 2001). The most dramatic figures however, are those from a study in Canada which estimated that 187 billion pollinators (mainly Hymenoptera) are killed over the summer in North America (Baxter-Gilbert et al., 2015).  An unpublished study by Roger Morris (thank you Richard Wilson @ecology_digest for bringing this to my attention) also highlights the dangerous effects of cars on Hymenoptera). Despite the mounting evidence of the harm that road traffic does to insects there is remarkably little information about how this can be reduced, although I did find a paper that noted that if insects are struck by cars driving at speeds of 30-40 km/h they survive the crash whereas speeds greater than this prove fatal (Rao & Girish, 2007).  It might be possible to impose insect safe speed limits along stretches of road that go through sites of special insect interest (perhaps I should try and coin that acronym, SSII, as an additional/alternative term to SSSI (Sites of Special Scientific Interest), but I am not sure how amenable drivers would be to signs telling them to slow down because of insects😊, considering how few drivers slow down in response to the signs warning them about deer and other vertebrate hazards. Another option would be to design road vehicles so that the air flow across them pushes insects away rather than into them; this may already be fortuitously happening as Manu Saunders points in her interesting post about the ‘windscreen anecdote’.  That said, even if cars are more aerodynamic and less likely to splatter insects, the levels of road kill reported in the papers I have cited earlier, still imply that insects are being killed by traffic in huge numbers.

This one didn’t get stuck on a car, but died just the same – A519 outside Forton, Staffordshire, 15^th June 2021

Even if we do accept that deaths down to direct impact with vehicles is lower than in the past, the roads on which we drive our cars are also having a negative effect on insect numbers. Roads, particularly those surfaced with tarmacadam, present an inhospitable surface to some insects which may make them reluctant to fly or walk across. It has been shown that bee and was communities can be different on different sides of a road (Andersson et al., 2017) as the road act as barriers, particularly for smaller species of bees (Fitch & Vaidya, 2021).

Despite the mortality that vehicles impose on insects, roads are not necessarily a totally bad thing for invertebrates; road verges, when sympathetically managed, can provide overwintering sites for a range of arthropod species (Saarinen et al., 2005; Schaffers et al., 2012) and some insect species seem to enjoy feeding on roadside vegetation because of the increased nitrogen content of the plants living alongside traffic (Jones & Leather, 2012).

Overall however, given the very high mortality rates directly associated with cars and other road traffic and the very real indirect effects caused by habitat fragmentation, it would seem that we have much to do to make roads safer for insects and other animals.

References

Andersson, P., Koffman, A., Sjödin, N.E. & Johansson, V. (2017) Roads may act as barriers to flying insects: species composition if bees and wasps differs on two sides of a large highway.  Nature Conservation, 18, 41-59.

Baxter-Gilbert, J.H., Riley, J.L., Neufeld, C.J.H., Litzgus, J.D., & Lesbarreres, D. (2015) Road mortality potentially responsible for billions of pollinating insect deaths annually. Journal of Insect Conservation, 19, 1029-1035.

Fitch, G. & Vaidya, C. (2021) Roads pose a significant barrier to bee movement, mediated by road size, traffic and bee identity. Journal of Applied Ecology, 58,1177–1186.

Glick, P.A. (1939) The Distribution of Insects, Spiders, and Mites in the air.  Technical Bulletin no. 673, USDA. https://naldc.nal.usda.gov/download/CAT86200667/PDF

Grout, A. & Russell, R.C. (2021)H Aircraft disinsection: what is the usefulness as a public health measure? Journal of Travel Medicine, 28, taaa124.

House, A.P.N., Ring, J.G., Hill, M.J. & Shaw, P.P. (2020) Insects and aviation safety: The case of the keyhole wasp Pachodynerus nasidens (Hymenoptera: Vespidae) in Australia. Transportation Research Interdisciplinary Perspectives, 4, 100096.

Jones, E.L. & Leather, S.R. (2012) Invertebrates in urban areas: a review. European Journal of Entomology, 109, 463-478.

McKenna, D.D., McKenna, K., Malcolm, S.B. & Berenbaum, M.R. (2001) Mortality of lepidoptera along roadways in Central Illinois. Journal of the Lepidopterist’s Society, 55, 63-68.

Melis, C., Olsen, C.B., Hyllvang, M., Gobbi, M., Stokke, B.G., & Røskaft, E. (2010) The effect of traffic intensity on ground beetle (Coleoptera: Carabidae) assemblages in central Sweden. Journal of Insect Conservation, 14, 159-168.

Munõz, P.T., Torres, F.P. & Megias, A.G. (2015) Effect of roads on insects: a review. Biodiversity & Conservation, 24, 659-682.

Pop, D.R., Maier, A.R.M., Cadar, A.M., Cicort-Lucaciu, A.S., Ferenți, S. & Cupșa, D. (2020) Slower than the trains! Railway mortality impacts especially snails on a railway in the Apuseni Mountains, Romania. Annales Zoologici Fennici, 57, 225-235.

Rao, R.S.P & Girish, M.K.S. (2007) Road kills: assessing insect casualties using flagship taxon. Current Science, 92, 830-837.

Reynolds, D.R., Chapman, J.W., Edwards, A.S., Smith, A.D., Wood, C. R., Barlow, J. F. and Woiwod, I.P. (2005) Radar studies of the vertical distribution of insects migrating over southern Britain: the influence of temperature inversions on nocturnal layer concentrations. Bulletin of Entomological Research, 95, 259-274.

Riffell, S.K. (1999) Road mortality of dragonflies (Odonata) in a Great Lakes coastal wetland. Great Lakes Entomologist, 32, 63-74.

Saarinen, K., Valtonen, A., Jantunen, J. & Saarnio, J. (2005) Butterflies and diurnal moths along road verges: does road type affect diversity and abundance? Biological Conservation, 123, 403-412.

Schaffers, A.P., Raemakers, I.P., & Sýkora, K.V. (2012) Successful overwintering of arthropods in roadside verges. Journal of Insect Conservation, 16, 511-522.

Unsolved mysteries or unasked questions? The mysterious case of the bumbling bibionids

Some years ago, Ole Heie published a paper discussing what he called aphid mysteries not yet solved (Heie, 2009).  These included such gems as the shark’s fin on the giant willow aphid and why are aphids so fussy about their host plants? I could add a few of my own; of the three very common aphids that feed on sycamore, one, Periphyllus testudinaceus, is commonly attended  by ants another P. acericola, is sometimes attended by ants and the third, Drepanosiphum platanoidis is attacked by ants. The question that one would ask is why this gradation when all three aphids live on the same tree and all produce lots of honeydew, the ant’s reward. People have pointed out that those ants that are obligately ant-attended have evolved a specific structure, the trophiobiotic organ (Heie, 1980) and that the siphunculi in non-ant attended aphids are longer than those of ant-attended species, which presumably enhances their defensive function (Way, 1963). These observations do not, however, answer the question as to why the association or lack of association arose, they just allow us to speculate about how the association has shaped the aphid, in essence an example of a circular argument.  Although I have raised the question, and you might respond and say that the question has been asked by voicing it, in my opinion, the question remains unasked (untested) and the mystery unsolved.  

There are plenty more aphid examples I could throw into the mix, but given the time of year when I started to write this, I thought I’d do a more topical unsolved mystery.  Why are St Mark’s flies (Bibio marci) so easy to catch? A simplistic answer is they are so easy to catch because they fly very slowly and appear to make no effort to avoid being caught.  I can literally grab them out of the air.  

One that I caught earlier -)

The real question is how come they are so easy to catch? Why, unlike the ubiquitous housefly, Musca domestica, which is nigh on impossible to sneak up on, (well by me at any rate, but perhaps you are better at it than me), has evolution produced such a dozy animal?  

Dipteran phylogeny (after Yeates et al., 2007). 

Bibionids appeared earlier in the evolution of flies than the Muscids and if you look at the phylogeny above you can see that as new Orders of flies arose, they moved from being long-legged, relatively clumsy fliers, such as the crane flies and Bibionids to the much more agile species we see in the Empids (dagger flies), Asilids (robber flies) and blue bottles and house flies.  Bibio marci is found across most of Europe while the housefly is found everywhere that humans are to be found, a truly global beast.  Based on distribution alone we could argue that M. domestica  is the more successful of the two. 

Their structure apart, are there any differences in their life history traits that might explain why natural selection has shaped adult Bibionids into being such easily caught organisms when compared with houseflies? Given the big differences in their flight agility we might expect their respective predators to be markedly different.  The eyes of a typical housefly have about 3400 ommatida (Sukontason et al., 2008) and process visual information around seven times more quickly than humans, enabling them to identify, and easily avoid attempts to catch or swat them, since they effectively see the human’s movements in slow motion. The eyes of bibionids on the other hand are divided into two halves, with one half pointing upwards, the other downwards.  The upward pointing half is used to locate mates while the downward pointing half is used for positioning (Zeil, 1983), so they are good at hovering (Ennos,1989), but not very agile in comparison with other flies, including, in my experience anyway, crane flies, which although looking clumsy are surpassingly good at not being caught*.  Despite these differences in flight ability, their predators are not very different.  Adult houseflies have many predators, including birds, reptiles, amphibians, various insects, and spiders which is pretty similar to St Mark’s flies, the adults of which form a substantial proportion of the diet of birds, such as starlings and chaffinches and are eaten by spiders and attacked by Empids (dagger flies) (D’Arcy-Burt & Blackshaw, 1991). 

What about their diets then? You might not realise it but we can describe adult houseflies as being mainly carnivorous; their primary food is animal matter, carrion, and faeces, but they also consume milk, sugary substances, and rotting fruit and vegetables. Although they don’t have jaws per se, they deal with solid foods by liquefying them with saliva before sucking it up.  Given their food preferences they are great at moving bacteria around the environment, hence their bad reputation as public health pests. Adult bibionids on the other hand are nectar feeders (Lewis & Smith, 1969; Smith & Lewis, 1972), so can be classified as beneficals due to their pollinating ability (Lewis & Smith 1969). As larvae, B. marci feed on leaf litter, both coniferous (von Schremer, 1958) and deciduous (Pobozsny, 1982), so again have a very important role in humification and soil formation (Pobozsny, 1982).  House fly larvae feed primarily on muck, dead and decaying material, animal faeces, pig manure being a particular favourite (Larrain & Salas, 2008; Pastor et al., 2011), which, like B. marci, makes them important components of the ecosystem. We are, however, concerned with the adults and their exposure to predators, and looking at their respective life styles it seems odd that B. marci is such a lethargic flyer as it would seem to be just as, or even more so, exposed to predators as the house fly.

That leaves us with the life cycle.  Is there something about B. marci’s life history traits that enables it shrug off the possibility of predation?  The adult has a short life cycle, one week, there is only one generation a year and the typical female lays 3330 eggs (Skartveit, 2002), so pretty prolific. The house fly has a longer adult life, and at 25^oC lays just over 700 eggs (Fletcher et al, 1990), so although fecund, nowhere near as productive as B. marci.   They do however, whip through the generations, in temperate regions of the world getting through 10-12 generations in a year, so their multiplication rate is massive compared with that of our bumbling bibionid.

Given all the evidence, I would have thought that B. marci would benefit greatly by being a faster flyer and less conspicuous and/or unpalatable.  It is none of these things. It might be spatially aware, but its predator avoidance mechanisms seem to leave a lot to be desired and birds love to eat it. That said, it has been remarkably successful and was, in the past, regarded as an agricultural pest (Morris, 1921).  There does, however, seem to be growing evidence, that B. marci is not as numerous as it once was, (Grabener et al., 2020), so given the close association that the house fly has with humans and the current direction of global heating, I would bet that the former will, over the next few years decline in numbers and the latter become an even bigger pest. Sadly, this seems to be the direction we are heading with regard to insect numbers, those we love are threatened, those we hate are doing well ☹

References 

 D’Arcy-Burt, S. & Blackshaw, R.P. (1991) Bibionids (Diptera: Bibionidae) in agricultural land: a review of damage, benefits, natural enemies and control. Annals of Applied Biology, 118, 695-708. 

Ennos, A.R. (1989) The kinematics and aerodynamics of the free flight of some Diptera. Journal of Experimental Biology,142, 49-85. 

Fletcher, M.G., Axtell, R.C., & Stinner, R.E. (1990) Longevity and fecundity of Musca domestica (Diptera: Muscidae) as a function of temperature. Journal of Medical Entomology, 27, 922–926.  

Grabener, S., Oldeland, J., Shortall, C.R. & Harrington, R. (2020) Changes in phenology and abundance of suction-trapped Diptera from a farmland site in the UK over four decades.  Ecological Entomology, 45, 1215-1219.

Healy K, McNally L, Ruxton GD, Cooper N, Jackson AL (2013). Metabolic rate and body size are linked with perception of temporal information. Animal Behaviour. 86, 685–696.  

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

Heie, O.E. (2009) Aphid mysteries not yet solved (Hemiptera:Aphidomorpha). Monograph Aphids and Other Hemipterous Insects, 15, 31-48. 

Larrain, P.S. & Salas, C.F. (2008) House fly (Musca domestica L.) (Diptera: Muscidae) development in different types of manure. Chilean Journal of Agricultural Research, 68, 192-197.

Lewis, T. & Smith, B.D. (1969) The insect faunas of pear and apple orchards and the effect of windbreaks on their distribution. Annals of Applied Biology, 64, 11-20.

Morris, H.M. (1921) The larval and pupal stages of the Bibionidae.  Bulletin of Entomological Research, 12, 221-232.

Skartveit, J. (2002) Variation in fecundity in relation to female size and altitude in Palaearctic Bibioninae (Diptera, Bibionidae). Studia Dipterologica, 9, 113-127. 

Smith, B.D. & Lewis, T. (1972) The effects of windbreaks on the blossom-visiting fauna of apple orchards and on yield. Annals of Applied Biology, 72, 229-238.

Sukontason, K.L., Chaiwong, T., Piangjai, S. et al. (2008) Ommatidia of blow fly, house fly, and flesh fly: implication of their vision efficiency. Parasitology Research, 103, 123–131. 

Pastor, B., Cickova, H., Kozanek, M., Martinez-Sanchez, A., Takac, P. & Rojo, S. (2011) Effect of the size of the pupae, adult diet, oviposition substrate and adult population density on egg production in Musca domestica (Diptera: Muscidae). European Journal of Entomology, 108, 587-596.

Pobozsny, M. (1982) The feeding biology of larval St Mark’s fly Bibio marci (Diptera: Bibionidae). Acta Zoologica Academie Scientiarum Hungariaicae, 28, 355-360.

von Schremer, F. (1958) Bibio larvae as utilisers of litter of dead needles. Anziger Schadlingskunde, 31, 151-153.

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

Yeates, D.K., Wiegmann, B.M., Courtney, G.W., Meier, R., Lambkin, C., & Pape, T. (2007) Phylogeny and systematics of Diptera: Two decades of progress and prospects. Zootaxa, 1668, 565-590. 

Zeil, J. (1983) Sexual dimorphism in the visual system of flies: the compound eyes and neural superposition in bibionidae (Diptera). Journal of Comparative Physiology, 150, 379-393.  

*I speak from bitter experience; my second-year undergraduate insect collection was Tipulids, which turned out to be a lot more difficult to catch than I had anticipated.

Green islands for the third and final time?

I have regaled you with tales of green islands twice before, first in relation to trees miraculously surviving mass defoliation events, and second, in terms of leaf miners and their exploitation of cytokinins.  This time it is the turn of the cowpat islets to make their appearance.  Those of you who are lucky enough to be able to walk in the countryside will probably have noticed that some of the fields you walk through are dotted with lots of clumps of longer grass and perhaps wondered what they are and why they are there.

A recently grazed pasture, showing very clear cowpat islets (Sutton, Staffordshire May 2021).

 If you look early enough or carefully later on, you will see that these clumps are associated with cowpats.  There have been a lot of theories about why these clumps arise, ranging from increased plant nutrition (Taylor & Rudman, 1966), after all we put manure on our gardens to improve plant growth, to unpalatability of the grass due to raised sugar levels (Plice, 1951).  This latter idea has since been dismissed, although the fact that cattle avoid feeding on these clumps has been well documented (Merten & Donker, 1964).  There is another explanation for why cattle avoid grazing near cowpats. You may not know it, but despite the fact that cattle don’t seem to have much control (or perhaps they just don’t care) over when and where they deposit their excreta, but cattle, despite the behaviour of bullocks, aren’t stupid. Just like you and me, they aren’t that keen on eating their own and other people’s sh*t.  A good reason for avoiding eating excreta, whether your own or someone else’s, is that areas contaminated with dung are associated with higher numbers of gastro-intestinal parasites (Boom & Sheath, 2008; Gethings et al., 2015), so it makes very good sense to avoid eating contaminated grass.  Whatever the reason, be it increased nutrition or distastefulness, the result is clumps of longer grass dotted around the pasture taking up between 20 and 30% of the field (Taylor & Rudman, 1966).

You may, by now, be wondering why an entomologist is going on about cowpats and grass clumps. Well, as you all know, in my world, everything comes round to entomology 🙂 It has been known for some time that hedges and hedgerows provide refuges for insects, admittedly, not all beneficial ones (Lewis, 1969; D’Hulster, M. & Desender, 1982), but nevertheless, an observation that led to the development of beetle banks and conservation headlands (Sotherton et al., 1989; Thomas et al., 1991). It is, however, not just field boundaries that can provide habitats for insects. Belgian coloepterist, the late Konjev Desender and colleagues, found that the sward islets provided extra overwintering sites for staphylinid beetles, which provide an important role in natural pest regulation (D’Hulster & Desender, 1984).  Strangely, well to me anyway, interest in the entomological role of sward islets died a death.  It wasn’t until almost thirty years later that a former colleague of mine, keen hemipterist Alvin Helden (now at Anglia Ruskin University), and colleagues, found that sward islets were also proving very important refugia for grassland Hemiptera and lycosid and linyphid spiders (Helden et al., 2010: Dittrich & Helden, 2012). Before the grazed sward recovered the islets, which in their study occupied 24% of the pasture, hosted about 50% of the total arthropod community.  So a very important role in conserving biodiversity within agroecosystems, but despite this very important finding, sward islet entomology has yet again fallen off the entomological radar 😦

Less recently grazed pasture, but cowpat islets still visible within the recovering sward (Sutton, Staffordshire, May 2021) but still, according to Alvin Helden, containing a higher density of arthropods than the surrounding grazed area (Helden et al., 2010).

I think that revisiting the ecology of sward islets would prove very rewarding for both MSc and PhD projects.  Off the top of my head I can come up with a couple of projects; for a PhD, given that the fertilisation level and type affected the relative abundance of two of the Hemipteran families, Delphacids and Cicadellids (Dittrich & Helden, 2012), a comparison of the fauna and flora of sward islets on conventional and organic farms would make a really rewarding project. Harking back to my interests in island biogeography a study of the size, floral composition, structure and distribution of sward islets and how this affects arthropod communities would make a neat MSc project or perhaps even another PhD.

I am sure that with a little bit of thought, many more projects, not just entomological could be devised. Over to you dear readers.

References

Boom, C.J. & Sheath G.W. (2008) Migration of gastrointestinal nematode larvae from cattle faecal pats onto grazable herbage. Veterinary Parasitology, 157, 260-266.

D’Hulster, M. & Desender, K. (1982) Ecological and faunal studies on Coleoptera in agricultural land III. Seasonal abundance and hibernation of Staphylinidae in the grassy edge of a pasture. Pedobiologia, 23, 403–414.

D’Hulster, M. & Desender, K. (1984) Ecological and faunal studies of Coleoptera in agricultural land IV. Hibernation of Staphylinidae in agro-ecosystems. Pedobiologia, 26, 65–73.

Dittrich , A.D.K. & Helden, A.J. (2012) Experimental sward islets: the effect of dung and fertilisation on Hemiptera and Araneae. Insect Conservation and Diversity, 5, 46–56.

Gethings, O.J., Sage, R.B. & Leather, S.R. (2015) Spatio-temporal factors influencing the occurrence of Syngamus trachea within release pens in the south West of England. Veterinary Parasitology, 207, 64-71.

Helden, A.J., Anderson, A., Sheridan, H. & Purvis, G. (2010) The role of grassland sward islets in the distribution of arthropods in cattle pastures. Insect Conservation and Diversity, 3, 291–301.

Lewis, T. (1969) The diversity of the insect fauna in a hedgerow and neighbouring fields. Journal of Applied Ecology, 6, 453-458.

Marten, G.C. &  Donker, J.D. (1964) Selective grazing induced by animal excreta. II. Investigation of a causal theory. Journal of Dairy Science, 47, 871-874.

Plice, M. J. (1951) Sugar versus the intuitive choice of foods by livestock. Agronomy Journal, 43, 341-342.

Sotherton, N.W., Boatman, N.D. & Rands, M.R.W. (1989) The ‘conservation headland’ experiment in cereal ecosystems. The Entomologist, 108, 135-143.

Taylor, J.C. & Rudman, J.E. (1966) The distribution of herbage at different heights in ‘grazed’ and ‘dung patch’ areas of a sward under two methods of grazing management. The Journal of Agricultural Science, 66, 29-39.

Thomas, M.B., Wratten, S.D. & Sotherton, N.W. (1991) Creation of ‘island’ habitats in farmland to manipulate populations of beneficial arthropods: Predator densities and emigration. Journal of Applied Ecology, 28, 906-917.

Data I’m never going to publish – factors affecting sycamore flowering and fruiting patterns

As a teenager I used to have a favourite thinking place, underneath a large beech tree half-way down the school drive.  I used to watch the activities of my school mates, while contemplatively chewing beech nuts (my school friends found this mildly disgusting).

Some years beech nuts were much easier to find than others; although I didn’t realise it at the time, this was my introduction to the phenomenon of masting.  At this point I had better fill you in on the basics of tree reproduction. Like most plants, trees reproduce by producing flowers that are pollinated, depending on the species, by vertebrates, insects or the wind. The fertilised flowers then produce seeds that are housed in what we term fruit or cones, and which in many cases aid their dispersal. Reproduction is energetically a costly process, reserves channelled to reproduction cannot be use for growth and defence.  Trees have evolved three different approaches to this problem. Some trees produce a moderate number of seeds in most years, others have an Irregular fruiting pattern and some, such as beech and oak, have strongly periodic fruiting patterns, “mast” years.  Interestingly (my wife hates me starting sentences off like this), trees that mast are wind pollinated.

Beech (Fagus sylvatica) mast production over a sixteen year period in England. Data from Hilton & Packham (1997

You might wonder why, if reproduction is costly, that some trees are ‘willing’ to expend so much energy in one go.  There are two schools of thought regarding this. One, which I find fairly convincing, is the “predator satiation” hypothesis (Janzen, 1971).  This basically says that the trees, by having on and off years, starve their specialist seed predators in the off years, thus reducing predator pressure by killing lots of them off. In the mast years, there are enough seeds to feed the surviving predators and produce another crop of trees.  A more recent, and less exciting suggestion (to me anyway), is that if the trees have a mass synchronised flowering effort, i.e. a mast year, then the chances of being pollinated are greatly increased (Moreira et al., 2014).

People tend to associate masting with trees that produce heavy fruit, acorns, hazel nuts and beech nuts for example, and I was no exception, so it wasn’t until a couple of years (1995) after I started my mega-sycamore study at Silwood Park that I had a bit of a revelation. I realised that not all of the trees flowered and that there seemed to be a lot fewer seeds that year than I remembered there being the year before. Sycamore seeds come equipped with two little wings (they are wing dispersed) and occur in little bunches (infructescences) so are quite noticeable.

Winged sycamore seed and ‘bunch’ of sycamore fruit

My sycamore study was one of my many side projects set up to satisfy my’ satiable curiosity’ and I had, at the time thought that I had made sure I was measuring everything that could possibly interact with the aphids feeding on the trees. I had, however, somehow overlooked sycamore flower production 🙂 I had taken into account that in some years the sycamore aphid can be present in huge numbers and and I was well aware from the work of my PhD supervisor

Sycamore aphids emerging in spring – some years you can see even more on the newly flushing buds

Tony Dixon, that the aphids can cause substantial losses to tree growth (Dixon, 1971), so had included tree girth and height measurements into my massive data collection list. Strangely, however, despite knowing from my work with

The effect of the sycamore aphid, Drepanosiphum platanoidis, on leaf area of two sycamore, Acer pseudoplatanus, trees over an eight year period (Dixon 1971).

the bird cherry-oat aphid Rhopalosiphum padi, that even quite low numbers of aphids could have substantial negative effects on cherry production (Leather, 1988), I had totally overlooked sycamore flowering and seed production. I am just thankful, that I only missed three years of flowering data 🙂

The effects of bird cherry aphid infestation on reproductive success of the bird cherry, Prunus padus (Leather, 1988)

Unlike the rest of my sycamore data set, the flowering data collection was actually set up to test a hypothesis; i.e. that aphid numbers affected flowering and seed set. Sycamore is in some ways similar to the well-known masting species such as oak and beech in that it is (jargon coming up) heterodichogamous. All flowers are functionally unisexual and appear sequentially on a single inflorescence. The inflorescences can however be either protandrous, i.e. male anthesis takes place before the stigmas become receptive, or protogynous where the reverse sequence takes place. Where it differs from the typical masting species is that is produces wind dispersed seeds and is wind and insect pollinated; oak, beech and hazel are entirely wind pollinated.  Pierre Binggelli, then based at the Unibersity of Ulster, hypothesised that protandrous trees may suffer less herbivore damage than protogynous trees (Binggeli, 1992). He suggested that protogynous trees, having less energy available to invest in defensive chemistry, are more attractive to insect herbivores, particularly chewers. On the other hand, sycamore trees that have been subject to previous insect infestation have fewer resources available to produce female flowers, become protandrous and avoid infestation by herbivores the following year. Presumably the next year, having escaped insect attack by being protandrous they should become protogynous again. So, if I wanted to test this hypothesis, I needed to learn how to sex sycamore flowers. Despite a handy guide that I came across (Binggeli, 1990), ) I found it almost impossible, to do, so

A. Protogynous inflorescence (female II flowers of Mode G are male II in Mode B). B. Protogynous infructescence, Mode B. C. Protogynous infructescence, Mode G. D. Protandrous inflorescence.
E. Protandrous infructescence. F. Vegetative shoot, G. Flowering shoot (Mode E).
H. Fruiting shoot (Flowering Modes B,C,D & G). (From Binggeli, 1990)

contacted Pierre, who very kindly agreed to check some of my ‘guesses’ for me.  Despite this help, I still found it very difficult so opted (very unwisely as it turned out) to collect fruit samples from each tree, put them in paper bags, and bring them back to the lab for sexing at a later date.  As you have probably guessed, I ended up with lots of paper bags which I then, not very cleverly, stored in plastic bin bags.  This went on for several years as I kept putting off the day when I would have to sit down and sex several thousand bunches of sycamore fruit. Then came the happy disastrous day when I came back from holiday to find out that the cleaners had disposed of my bin bags. To tell the truth I was not that upset as it gave me an excuse to stop collecting the fruit samples and reduced my feelings of guilt about having huge piles of unsexed sycamore fruit bunches cluttering up the lab 🙂 I did, of course, carry on counting the number of flowers on the trees, which was much easier data to collect and analyse.

I reluctantly ended my study in 2012 when I left Silwood Park for pastures new, but despite this I still haven’t analysed all my sycamore data, although I was very happy a couple of years ago when a PhD student from the University of Sheffield (Vicki Senior) volunteered to analyse some of my sycamore aphid data which was published last year (Senior et al., 2020). The winter moth data and orange ladybird data are also being analysed by a couple of my former students and hopefully will also be published by next year.

So what does the sycamore fruiting data show? Well, first, despite sycamore being reproductively somewhat atypical of other masting trees species, I would contend that my 17-year data set of sycamore fruit production looks remarkably similar to the Hilton and Packham beech masting data set. I am thus confident in stating that sycamore is a masting species.

Mean sycamore fruit production at Silwood Park, averaged from 52 trees 1996-2012,

Am I able to link sycamore seed production with aphid abundance, is the fruiting pattern a result of herbivory?  I can’t test Pierre Binggeli’s hypothesis about sex changing trees, because I lost the data, but I can try and see if aphid infestation affects fruit production. The two most common aphid species on the Silwood Park sycamore trees are the sycamore aphid Drepanosphum platanoidis and the maple aphid, Periphyllus acericola.  

Mean sycamore aphid and mean maple aphid loads (average annual counts per 40 leaves from all trees) 1996-2012.

They can both occur in high numbers, but in general, the average numbers of P. acericola are much higher than D. platanoidis. The reason why P. acericola has much higher numbers is a result of its over-summering strategy.

Over-summering morphs of the sycamore and maple aphid. Images from https://influentialpoints.com/Gallery/Drepanosiphum_platanoidis_common_sycamore_aphids.htmhttps://influentialpoints.com/Gallery/Periphyllus_acericola_Sycamore_Periphyllus_Aphid.htm#other

While the sycamore aphid spends the summer aestivating (basically a summer version of hibernation in that metabolism is reduced and reproduction ceases), the maple aphid produces a huge number of nymphs, known as dimorphs, which over-summer in dense, immobile aestivating colonies.  The sycamore aphid can escape predators by flying off the leaves if disturbed, the maple aphid dimorphs on the other hand, rely on their huge numbers to ensure survival of some of them over the summer to resume development and reproduce as autumn approaches, a form of predator satiation. They thus suffer a huge reduction in numbers compared with the sycamore aphid. (I must publish that one day). This makes drawing conclusions about the of herbivory (aphid feeding) on the trees a bit difficult.

Mean combined aphid load, showing how the number of dimorphs of the maple aphid skew the perceived aphid load.

Given that Tony Dixon showed that sycamore aphids cause a significant reduction in tree growth (Dixon, 1971), I

Relationship between mean combined aphid load (sycamore and maple aphid) and mean sycamore fruit production.

expected to see a negative relationship between aphid numbers and fruit production. What I did find was that there was a significant positive relationship between sycamore aphid numbers and fruit production, i.e. the more sycamore aphids, the more fruit produced, whereas with the maple aphid it was the other way round, more maple aphids, fewer fruit. If I combined the aphid loads, then the relationship becomes significantly positive, the more aphids you get the

Relationship between mean combined aphid load and the number of sycamore fruit produced the following year.

significantly negative relationship between aphid numbers and sycamore fruit production, but as I pointed out earlier this is driven by the preponderance of maple aphid dimorphs in the summer. You might also argue, that rather than looking at aphid numbers and sycamore fruit production in the same year, I should be comparing aphid numbers with fruit production the following year, i.e. a lag effect. I did indeed think of this, and found that there was, for both aphid species, no significant relationship between aphid numbers the previous year and fruit produced the following year. In fact, if I was an undergraduate student I would point out that there was a positive trend between aphid numbers and fruit production 🙂  If I do the same analysis using the combined aphid load, then the relationship becomes significantly positive, the more aphids you get the more sycamore fruit you get the following year which although counter-intuitive fits with the idea that stressed trees tend to produce more offspring (seeds) (Burt & Bell, 1991) and given that we know from Tony Dixon that the sycamore aphid causes a significant reduction in growth (Dixon, 1971) which is an indication of plant stress (Grime, 1979) makes perfect sense. 

Relationship between mean combined aphid load and the number of sycamore fruit produced the following year.

Instead of mean aphid load, perhaps we ought to be thinking about aphid occurrence at crucial times of the year for the tree, for example budburst. If you go back to the top of the page and look at the photograph of the infested buds you can see that there can be a huge number of aphids present at this time of year just when the trees are starting to wake up and put on new growth. Any interference to the uptake of nutrients at this phase of their life cycle could be detrimental to fruit production.  One way to measure this is by looking at the date the first aphids appear on the buds in the expectation that the earlier the aphids start to feed, the bigger their impact on the trees. Sure enough, the earlier the aphids start feeding, the lower the number of fruit produced.

Significant negative relationship between date of first appearance of aphids on the buds and number of fruit produced in spring.

Although all the relationships I have discussed and shown are significant, the amount of variation is explained is pretty low (over 20% but less than 30%). The relationship that explains most of the variation in any one year is the size of the tree, the bigger the tree the more fruit it produces.

Relationship between size of sycamore tree and number of fruit produced (2009).

As a rule of thumb, the bigger a tree the older it is and older trees have more resources and can afford to produce more offspring than younger smaller trees.

In conclusion, what I can say with confidence is that there is significant variability in sycamore fruit production between years and this is, in my opinion, evidence of masting events, and may be linked to the size and timing of aphid load but is moderated by the size and age of the trees. If you have any other suggestions please feel free to add them in the comments.

If anyone is interested in delving into the data in more depth I will be very happy to share the raw data and also the local weather data for the site.

References

Binggeli P. (1990) Detection of protandry and protogyny in sycamore (Acer pseudoplatanus L.) from infructescences. Watsonia,18, 17-20.

Binggeli P. (1992) Patterns of invasion of sycamore (Acer pseudoplatanus L.) in relation to species and ecosystem attributes. D.Phil. Thesis, The University of Ulster.

Burt, A. & Bell, G. (1991) Seed production is associated with a transient escape from parasite damage in American beech.  Oikos, 61,145–148.

Dixon, A.F.G. (1971) The role of aphids in wood formation. 1. The effect of the sycamore aphid, Drepanosiphum platanoides (Schr.) (Aphididae) on the growth of sycamore. Journal of Applied Ecology, 8, 165-179.

Hilton, G.M. & Packham, J.R. (1997) A sixteen-year record of regional and temporal variation in the fruiting of beech (Fagus sylvatica L.) in England (1980-1995). Forestry, 70, 7-16.

Hilton, G.M. & Packam, J.R. (2003) Variation in the masting of common beech (Fagus sylvatica L.) in northern Europe over two centuries (1800-2001). Forestry, 76, 319-328.

Janzen, D. H. (1971) Seed predation by animals. Annual Review of Ecology and Systematics, 2,465–492.

Leather, S.R. (1988) Consumers and plant fitness: coevolution or competition? Oikos, 53, 285-288.

Leather, S.R. (2000) Herbivory, phenology, morphology and the expression of sex in trees: who is in the driver’s seat? Oikos, 90, 194-196.

Moreira, X., L. Abdala-Roberts, Y. B. Linhart, and K. A. Mooney. (2014_. Masting promotes individual- and population-level reproduction by increasing pollination efficiency.Ecology, 95, 801–807.

Grime ., J.P. (1979) Primary strategies in plants, Transactions of the Botanical Society of Edinburgh, 43,2, 151-160.

Senior, V.L., Evans, L.C., Leather, S.R., Oliver, T.H. & Evans, K.L. (2020) Phenological responses in a sycamore-aphid-parasitoid system and consequences for aphid population dynamics; A 20 year case study. Global Change Biology, 26, 2814-2828.

Let your dandelions and other flowering ‘weeds’ be

This last couple of weeks parts of my daily walks have been accompanied by, the to me, unwelcome din of motor lawnmowers as lots of my fellow villagers strive to turn their lawns into ecological deserts. One of my neighbours has, to my knowledge, cut his lawn five times since the beginning of March, me I’ve done my spring cut and that’s it until autumn.

An ecological desert 😦

This mania for close-cropped lawns, sometimes ‘artistically’ striped, is, I think, the fault of my grandparent’s generation, which took a municipal park attitude to gardens, especially the bit that the neighbours could see; close-cropped, weed-free grass with regimented flower beds, also equally weed-frees. Out of sight, back gardens could be less manicured, and depending on the space available, might include a vegetable garden (also scrupulously weed-free), and a patch of lawn to be used by children for ball games and other activities. Unfortunately they drummed this philosophy into their children, who in their turn, with only a few exceptions (me for one), passed this fetish on to my generation. Sadly, my father, a keen gardener, also espoused this view as did the parents of all my friends. I spent many a grumpy hour removing dandelions and thistles from our front lawn and flower beds at my father’s behest!

So what are these weeds that so many people seem to hate? To those growing crops of economic value, be they agricultural, horticultural or silvicultural, then I guess the following definitions are very reasonable and relatable.

“Plants that threaten human welfare either by competing with other plants that have food, timber of amenity value, or by spoiling and thus diminishing the value of a product”

“Weeds arise out of the mismatch between the habitats we create and the plants we choose to grow in them”

Begon, Harper & Townsend (1996)

“A plant that originated under a natural environment and, in response to imposed and natural environments, evolved and continues to do so as an interfering associate with our desired plants and activities” Aldrich & Kremer (1997)

There are more tolerant descriptions of weeds available, which are much more in accord with my views:

What is a weed? A plant whose virtues have not yet been discovered” (Emerson, 1878)

, “A weed is but an unloved flower!” (Wilcox, 1911)

”A plant condemned without a fair trial” (de Wet & Harlan, 1975)

I have, as I have mentioned several times already, been doing a lot of walking during the covid pandemic, or should it now be referred to as the Covid Pandemic? At this time of year, Spring, the early flowers of the hedgerows and roadside verges are alreday out; cherry plum (Prunus cerasifera), blackthorn or sloe (Prunus spimosa) and closer to the ground, but as equally pretty, daisies (Bellis perennis), dandelions (Taraxacum officinale), Lesser Celandines ( Ficaria verna (although some of you may know it as Ranunculus ficaria), and Wood Anemones (Anemonoides nemorosa). The latter two species, although relatively common, are unlikely to be found in the average garden, as they have fairly specific habitat requirements.  Daisies and dandelions on the other hand, are pretty much ubiquitous, although the former do not attract as much opprobrium from the traditional gardener as dandelions do. This is a great shame, as ecologically speaking dandelions are an extremely important resource for pollen and nectar feeding insects.

Given the concerns about the decline of insects in general over the last forty years, we should be celebrating the dandelion, not trying to eradicate it from our lawns. Just feast your eyes on some of the beauties that I have seen over the last few days.

Pollen beetles March 20^th 2021

Male tawny mining bee Andrena fulva – Sutton March 25^th 2021

Bumble bee, Sutton March 30^th 2021

Seven spot lady bird, too early for aphids, Oulton Road March 30^th 2021

Peacock butterfly in a very striking pose, Guild Lane, Sutton, April 3^rd 2021.

I’m not alone in my love of dandelions 🙂

We shouldn’t forget the humble daisy either. It provides nectar to many butterfly species, including among others, the Green Hairstreak, the Grizzled Skipper, the Small Copper and the Small White. They are also important resources for honey bees (Raquier et al., 2015), bumblebees and hoverflies (Blackmore & Goulson, 2014).

A nice patch of daisies.

Domestic gardens, if managed correctly, have tremendous potential as reservoirs of insects and other invertebrates of ecological importance (Davies et al, 2009). The easiest thing that you can do to help the insects is to reduce the frequency at which you mow your lawn and grass verges. To sum it up in a nutshell, the less you move, the more flowers you get and the more flowers you get the more nectar and pollen feeding insects you make happy, some of which can be rare and endangered (Wastian et al., 2016).  

The less frequently you mow, the more flowers you get. The more flowers you get, the more bumblebees you get (George, 2008).

It is not just flower feeding insects that benefit from reducing your lawn mowing activities; grass feeding insects also benefit from longer grass ( Helden & Leather, 2005) and if, for some strange reason, you are not a great fan of bugs, just remember that the more bugs you have the more birds you will attract (Heden et al.,  2012). So do your bit to save the planet, be like me, only mow your lawn twice a year.

References

Aldrich, R.J. & Kremer, R.J. (1997) Principles in Weed Management. Panima Publishing Corporation.

Begon, M., Harper, J,L. & Townsend, C.R. ( 1996) Ecology, 3^rd Edition, Blackwell Science, oxford.

Blackmore, L.M. & Goulson, D. (2014) Evaluating the effectiveness of wildflower seed mixes for boosting floral diversity and bumblebee and hoverfly abundance in urban areas. Insect Conservation & Diversity, 7, 480-484.

Davies, Z.G., Fuller, R.A., Loram, A., Irvine, K.N., Sims, V. & Gaston, K.J. (2009) A national scale inventory of resource provision for biodiversity within domestic gardens. Biological Conservation, 142, 761-771.

De Wet, J.M.J., Harlan, J.R.  (1975) Weeds and domesticates: Evolution in the man-made habitat. Economic Botany, 29, 99–108.

Emerson, R.W.(1878) The Fortunes of the Republic. The Riverside Press, Boston, USA.

Garbuzov, M., Fensome, K.A. & Ratnieks, F.L.W.  (2015)   Public approval plus more wildlife: twin benefits of reduced mowing of amenity grass in a suburban public park in Saltdean, UK. Insect Conservation & Diversity, 8, 107-119.

George, W. (2008) The Birds and the Bees: Factors Affecting Birds, Bumblebees and Butterflies in Urban Green Spaces, MSc Thesis, Imperial College, London.

Helden, A.J. & Leather, S.R. (2005) The Hemiptera of Bracknell as an example of biodiversity within an urban environment. British Journal of Entomology & Natural History, 18, 233-252.

Helden, A.J., Stamp, G.C. & Leather, S.R. (2012) Urban biodiversity: comparison of insect assemblages on native and non-native trees. Urban Ecosystems, 15, 611-624.

Lerman, S.B., Contostac, A.R., Milamb, J. & Bang, C. (2018) To mow or to mow less: Lawn mowing frequency affects bee abundance and diversity in suburban yards. Biological Conservation, 221, 160-174.

Requier, F., Odoux, J., Tamic, T.,Moreau, N., Henry, M., Decourtye, A. & Bretagnolle, V. (2015)  Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weedsEcological Applications, 25, 881–890.  

Wastian, L., Unterweger, P.A.& Betz, O. (2016) Influence of the reduction of urban lawn mowing on wild bee diversity (Hymenoptera, Apoidea). Journal of Hymenoptera Research, 49, 51–63.

Wilcox, E.W. (1911) Poems of Progress and New Thought Pastels. London: Gay & Hancock, 1911.

Bee’s knees, a gnat’s whisker, knee-high to a grasshopper, a flea in your ear and other insect idioms

Idiom a group of words established by usage as having a meaning not deducible from those of the individual word

I’m fond of saying that I have been an entomologist since I was knee-high to a grasshopper, which I automatically expect my audience to understand means since I was very young.

Knee-high to a grasshopper?

What I didn’t know was that this well known phrase only dates from about 1850 and replaced the earlier knee-high to a mosquito or bumblebee or splinter. I can find no explanation as to why this change occurred; perhaps it was because someone felt sorry that the Orthoptera didn’t have any idioms associated with them as opposed to the Hymenoptera which dominate the insect idiom world.  “Rightly so” I can hear the Hymenopterists exclaiming, “after all there are more of them than any other Order” (Forbes et al., 2018).

Hymenoptera

When I go into the Entomology Lab I expect it to be a “hive of activity” where everyone is as “busy as a bee” and there is a “real buzz”.

Strangely enough, despite the hymenopteran references I would hope that my students are all working on aphids, but then some people would say that I have “a bee in my bonnet” about them and I will definitely be making “a beeline” to the aphid cultures shortly after I arrive as I think that aphids are the “bee’s knees” when it comes to insects 🙂 I can get quite

“waspish” when I hear people making disparaging remarks about aphids although I would never describe myself as getting as “mad as a hornet” over the matter. In fact I love aphids so much that if someone asks me why I do, I will never say “none of your beeswax” and you might think that I “have ants in my pants”  as I wait for an opportune moment to explain about the “birds and the bees” when applied to aphid reproduction.

Diptera

Erica McAlister author of The Secret Life of Flies will tell you that flies are where it’s at and it is certainly worth being “a fly on the wall” when Erica starts talking about flies in general.

Unless you have “the attention span of a gnat” you will be enthralled by her anecdotes. The only “fly in the ointment” is that some of her flies have absolutely disgusting habits.  Erica herself, “wouldn’t hurt a fly”, no matter how unsavoury its lifestyle. I have heard it said, that sometimes, the less strong-stomached members of her audience, can be seen “dropping like flies”.  I confess that I am a bit worried that if Erica reads this I will come within a “gnat’s whisker” of being slapped in the face 🙂 Speaking of gnats, I just found this expression in a detective novel published in 1932 (Wilkinson, 1932) “antiquated gnat of a custom”, but have not been able to find out exactly what it means and its origin – any suggestions welcomed.

Lepidoptera

No one could describe me as being as “gaudy as a butterfly” as my usual attire is a pair of blue jeans, a shirt with rolled up sleeves and a pair of desert boots, although I do have some butterfly-themed clothing.

Gaudy as a butterfly – nope

The previous sentence reminds me that I have written about dress codes in an earlier post,  and the role this might have in curing the feeling of “having butterflies in one’s stomach” before giving a talk. Speaking of nervousness coupled with shyness, something many of us feel in social situations, which can cause some of us to imbibe liquids containing alcohol, I find that even after a few drinks I am not much of a “social butterfly”, a garrulous drunk is probably the best description 🙂

Everything got a little bit hazy

Coleoptera

Now you might think that the Coleoptera, having, at the moment, the most species described would have provided us with a plethora of beetle inspired idiomatic expressions. Sadly as I “beetle along” in my “beetle crushers” I very soon come to the end of their influence on idiomatic English.  Just to make any coloepterist who might be reading this feel a bit better, the narrator in Rudyard Kipling’s Stalky & Co (a humorous novel about late Victorian schoolboys) is nicknamed Beetle, possibly because Kipling, like me, could be described as “beetle-browed”.

Beetle-browed, although my wife has been known to describe them as looking like furry caterpillars

Siphonoptera (Mecoptera)

Leaving the beetles behind us we come across the Siphonoptera, the fleas. Some people might say I have “a mind like a flea” but did you know that fleas have been recently re-classified as parasitic scorpionflies (Tihelka et al., 2020), which might make those people who say they “wouldn’t hurt a flea” think twice about using that phrase or the term “fleabag”.

Insects in general

As someone whose favourite insects are Hemipteran, I would love to say that the greatest number of insect idioms are provided by the true bugs, but that would be untrue. In general, when non-entomologists use the word bug, they mean insects in general, a particular “bugbear” of mine. I would go as far as to say that it really “bugs me”. In fact, I’d love to put “a bug in someone’s ear” about it and if I came across a journalist using bugs correctly I’d certainly go “bug-eyed”. I’m writing this in my warm centrally-heated house, feeling as

Not only snug as a bug but an example of one of my bugbears!

“snug as a bug in a rug” although once this pandemic is over I’m pretty sure that the “travel bug” will bite me, and I’ll be heading off to France to enjoy great food, good wine and plenty of sunshine.

References

Forbes, A.A., Bagley, R.K., Beer, M.A. et al. (2018) Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecology, 18, 21.

Tihelka , E., Giacomelli, M.,Huang, D., Pisani, D., Donoghue, P.C.J. &  Cai, C. (202o) Fleas are parasitic scorpionflies. Palaeoentomology,3, 641–653.

Wilkinson, E. (1932) The Division Bell Mystery, George Harrap & Co Ltd, London. Reprint available via the British Library Crime Classics series

Glossary

Hymenoptera

a bee’s dick – a very small amount https://stronglang.wordpress.com/2017/08/21/a-new-cooking-measurement/

a hive of activity – a place/situation where everyone is busy

ants in your pants/antsy – agitated or restless due to nervousness or excitement

as busy as a bee – very busy

as mad as a hornet – very angry

bee’s knees – an excellent person or thing, of the highest quality

birds and the bees – a euphemism for the basic facts about reproduction as told to a child

none of your beeswax – none of your business

to have a bee in one’s bonnet – to be preoccupied/obsessed with something

to make a beeline – to move swiftly and directly towards something or someone

Diptera

dropping like flies – dying or collapsing in large numbers, giving up on or pulling out of an endeavour

fly in the ointment – a small problem which nonetheless spoils the whole plan

fly on the wall – an unnoticed witness

wouldn’t hurt a fly – used to emphasize how inoffensive and harmless a person or animal is

Lepidoptera

as gaudy as a butterfly – very colourful

social butterfly – a person who is socially dynamic, successful at networking, charismatic, and personally gregarious

to have butterflies in one’s stomach – to feel nervous/anxious/excited in your stomach

Coleoptera

Beetle along – hurry, scuttle

Beetle-browed – having shaggy and projecting eyebrows

Beetle crushers – large shoes/boots

Siphonoptera (Mecoptera)

a flea in (someone’s) ear – an unwelcome idea or answer

mind like a flea – jumping from one idea to another

fleabag – a dirty or shabby person or animal, typically one infested with fleas or a seedy and dilapidated hotel

wouldn’t hurt a flea – gentle and kind

Insects in general

as snug as a bug (in a rug) – very comfortable/cosy

bug-eyed – with bulging eyes, astonished, amazed

to bug someone – to annoy someone

to put a bug in someone’s ear about something – to give someone a hint about something

travel bug – a strong desire to travel; an obsessive enthusiasm for or addiction to travellin;

Large, complex, beautiful and multi-chambered – Robin’s pincushion, rose bedeguar gall, mossy rose gall

As I wrote a little while ago, thanks to the Covid-19 lockdown I have been roaming the countryside around my rural retreat a lot more than I normally do. One of the things that I have noticed is that there seem to be a lot more of the spectacular galls caused by the gall wasp, Diplolepis rosae, than I can remember seeing in previous years. I have absolutely no empirical evidence for this observation, so it could all be down to shifting baselines (Jones et al., 2020). Nevertheless, to me they have been much more noticeable this year, perhaps confounding the insect apocalypse narrative (Leather, 2018), but then again, perhaps not.

I am, when it comes to galls, more of an expert on those caused by aphids, than on those induced by Hymenoptera, although, as it happens I am a co-author on an oak gall wasp paper (Walker et al., 2002).  Of course, that does not make me an expert. One the rose bushes in our front garden always has at least one of Robin’s spectacular pincushions clamouring for attention.  The others rarely have one and I have idly wondered about the host preferences of the wasp and the suitability of different roses for the development of the larvae.

Our front garden Diplolepis rosae gall

Having noticed that despite the relative abundance of the galls in the hedgerow roses, some bushes were totally gall-free while others supported several, sometimes in close proximity to each other, my thoughts immediately turned to possible student project.

Multiple infestations of Diplolepis rosae on hedgerow roses in the environs of Sutton, Staffordshire

A preliminary bit of research with the aid of Google Scholar quickly disabused me of that idea, but, as is the way with the internet, soon had me delving deep into the past in search of the history of this fascinating manifestation of insect activity.

My first discovery was that is also known as the rose bedeguar gall, something that had, until now, totally passed me by. According to my favourite dictionary (Gordh & Headrich, 2001),

“Bedeguar, Bedegar or Bedequar’ comes from a French word, bédégar, and is ultimately from the Persian, bād-āwar, meaning ‘wind-brought’”.

I’m guessing this meant that the first people to see them had no idea what caused them.

Not just complex galls

My next discovery was that D. rosae and the parasitoids that share its gall is a fairly well studied system (Randolph, 2005; Urban, 2018), although I am sure that it would still be possible to come up with some sort of project.  Diploelpis rosae is a member of the order Hymenoptera, so related to the larger and much more obvious bees, wasps and ants. It belongs to a family of wasps, the Cynipidae, commonly known as gall wasps.  Considering how small they are, 3.8 mm (Urban, 2018), the galls they make are spectacularly huge as are those that their relatives on oak form. Interestingly* more than 80% of gall wasps are associated with oaks, with most of the rest forming galls on members of the rose family (Shorthouse, 1973).  That in itself is, at least to me, an interesting fact; why such a restricted host range?  It is univoltine (one generation a year), overwinters as mature larva or pre-pupa in the galls, and emerges as adults in the spring when it seeks out suitable egg-laying sites. It is mainly parthenogenetic, although males are occasionally found (Callan, 1940; Stille, 1984). Despite being tiny, each wasp has the potential to lay about 500 eggs (Stille & Dävring, 1980). The adults are not very adventurous, usually laying eggs in the developing buds or flowers of the bush they emerged on, or on another close by (Bronner, 1985: Urban, 2018). That said, there must be some sort of host preference and selection going on, as in Sweden and the Czech Republic most galls are found on Rosa canina (Stille, 1984; Urban 2018). They also seem to favour younger bushes, or those that produce long vigorous stems (Stille, 1984).  The potentially high fecundity is presumably an adaptation to the high rates of parasitism that the larvae of D. rosae can experience, up to 70% in some cases (Stille, 1984).  In fact, so varied and numerous are the parasites, that many of the early papers about D. rosae pay more attention to the other inhabitants of the galls than they do the architects (Osten Sacken, 1870; Blair, 1945; Bugbee, 1951).  Females that lay a lot of eggs in the same developing bud produce bigger galls and a greater proportion of the larvae survive (Stille, 1984).

Survival of D. rosae in relation to gall weight (after Stille, 1984)

 It also appears that the closer to the ground the galls are, the lower the parasitism rate (Laszló, 2001).

The ideal strategy would then be for female D. rosae to lay big galls as low down on the plants as possible, but from personal observation this is not always the case , so as is often the case with the “Mother knows best” hypothesis there is something we humans are missing that the insects aren’t (Awmack & Leather, 2002).

Those darned taxonomists!

So, as so much is already known about this tiny wasp and its spectacular gall, I thought I would do a little bit of entomological archaeology and trace the entomological history of this little insect. Now I think taxonomists are wonderful people and have a huge respect for the very often unacknowledged work that they do, and am a great supporter of the campaign to make sure that people cite them in their papers (Packer et al., 2018), but they are a contentious bunch :-).  I mention this because inputting Diplolepis rosae into Google Scholar didn’t get me very far back in time, 1951 to be precise (Bugbee, 1951).  This paper justifies my good-natured jibe at the argumentative nature of taxonomists as he explains his renaming of what was then Rhodites rosae, by citing a 1917 paper (Rohwer & Fagan, 1917) who argued that the French entomologist Étienne Geoffroy (1725-1810) who raised the Genus Diplolepis in 1762, should take precedence over Theodor Hartig’s (1805-1880) 1840 Genus Rhodites. This pointed me back to the 1940s and the discovery that the mossy rose gall was then known as Rhodites rosae and I quote “I have recently published an epitome of  my own experience e in rearing from galls of R. rosae” (Blair, 1945). A bit more delving and I found that in France in the 1930s and in the USA in the 1920s, it was still known as R. rosae (Weld, 1926; da Silva  Tavares, 1930). Wending my back via citations I arrived in 1903 to find it listed as Cynips rosae (Ashmead, 1903).

Historical insights – Monsieur Wirey was ahead of his time

Armed with this knowledge, my journey back into the history of D. roase was much simplified and introduced me to a gem of a book, Insect Architecture by James Rennie  (1787-1867) (Rennie, 1851). Here I found an interesting account of galls in general but a detailed exposition of the Bedeguar gall of rose as he described it, including this rather nice drawing.

Professor Rennie presents some hypotheses on the formation of insect galls in general;

“Many of the processes which we have detailed bear some resemblance to our own operations of building with materials cemented together; but we shall now turn our attention to a class of insect-architects, and who cannot, so far as we know, be matched in prospective skill by any of the higher orders of animals. We refer to the numerous family which have received the name of gall-flies,

1. Wirey says, the gall tubercle is produced by irritation, in the same way as an inflamed tumor in an animal body, by the swelling of the cellular tissue and the flow of liquid matter, which changes the organization, and alters the natural external form. This seems to be the received doctrine at present in France. “

As you can see from the above he has little time for the French explanation (typical English exceptionalism) and puts forward his own idea that the galls are formed because the egg laying process blocks the vessels of the plant and the fluid that would normally flow unimpeded blows up the tissue surrounding the egg like a balloon.  Of course he was wrong and M. Wirey was correct :-).  Considering that he had no access to the sophisticated techniques we have he pretty much hit the nail on the head.

That aside, his book introduced me to an entomologist I had never heard of, Priscilla Wakefield (1751-1832), yet another overlooked and forgotten female scientist.

Possible projects?

Although my plans for lots of great MSc projects were reduced somewhat I have had a lot of educational fun and I think that there are still some things that could usefully be looked at, long term recording across multiple sites which I hope the British Plant Gall Society is doing would be interesting.  On my walks I noticed a lot of variability in size and phenology of gall formation.  At the end of August I was coming across small very fresh looking galls at the same time as I was seeing larger more advanced galls.

A very fresh looking Bedeguar gall, August 26^th 2020, Sutton

As far as I can tell, the timing of gall formation and its effect on final size of the galls has not been looked at in detail; do early galls enter winter larger than later formed galls, or is it entirely due to the number of eggs laid?  Given the huge number of other inhabitants of the galls, at least fourteen different species (Laszló, 2001, there is probably a viable project in looking at the timing of invasion by the different gall parasites and the outcome this may or may not have on the final composition of the gall fauna.

Feel free to suggest additional projects in the comments.

References

Ashmead, W.H. (1903) Classification of the gall-wasps and the parasitic cynipoids, or the superfamily Cynipoidea. IV, Psyche, 10, 210-216.

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

Blair, K.G. (1945) Notes on the economy of the rose‐galls formed by Rhodites (Hymenoptera, Cynipidae). Proceedings of the Royal Entomological Society, Series A, 20, 26-31.

Bronner, R. (1985) Anatomy of the ovipositor and oviposition behavior of the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae). Canadian Entomologist, 117, 849-858.

Bugbee, R. E. (1951). New and described parasites of the genus Eurytoma illiger from rose galls caused by species of the cynipid genus Diplolepis Geoffrey Hymenoptera: Eurytomidae). Annals of the Entomological Society of America, 44, 213–261

Callan, E.Mc. (1940) On the occurrence of males of Rhodites rosae (l.) (Hymenoptera, Cynipidae). Proceedings of the Royal Entomological Society of London, Series A., 15, 21-26.

Da Silva Tavares, J. (1930) Quelques Cécidies du Centre de la France, Publications de la Société Linnéenne de Lyon, 75, 145-167.

Gordh, G & Headrick, D.H. (2001) A Dictionary of Entomology, CABI, Wallingford

Jones, L.P., Turvey, S.T.,  Massimino, D. & Papworth, S. K.(2020) Investigating the implications of shifting baseline syndrome on conservation. People & Nature,

Laszló, Z. (2001) The parasitic complex of Diplolepis rosae (LinnaeuS, 1758) (Hymenoptera, Cynipidae): influencing factors and interspecific relationships. Entomologica Romanica, 6, 133–140.

Leather, S.R. (2018) “Ecological Armageddon” – more evidence for the drastic decline in insect numbers. Annals of Applied Biology, 172, 1-3.

Osten Sacken, R. (1870) Contributions to the natural hstory of the Cynipidæ of the United State and their galls.  Transactions of the American Entomological Society, 3, 54-64.

Packer, L., Monckton, S.K., Onuferko, T.M. & Ferrari, R.R. (2018) Validating taxonomic identifications in entomological research. Insect Conservation & Diversity, 11, 1-12.

Randolph, S. (2005) The Natural History of the Rose Bedeguar Gall and its Insect Community, The British Plant Gall Society.

Rennie, J. (1857) Insect Architecture. John Murray, London.

Rohwer, S. A. & Fagan, M. M. (1917) The type-species of the genera of the Cynipidea, or the gall wasps and parasitic cynipoids. Proceedings of the U.S. National Museum, 53, 357-380.

Shorthouse, J.D. (1973) The insect community associated with rose galls of Diplolepis polita (Cynipidae, Hymenoptera). Quaestiones Entomologicae, 9, 55-98.

Stille, B. (1984) The effect of hosptlant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae (Hymenoptera, Cynipidae). Oecologia, 63, 364-369.

Stille, B. & Dävring, L. (1980) Meiosis and reproductive strategy in the parthenogenetic gall wasp Diplolepis rosae (L.) (Hymenoptera, Cynipidae), Heriditas, 92, 353-362.

Urban, J. (2018). Diplolepis rosae (L.) Hymenoptera: Cynipidae): development, ecology and galls in the Brno region. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 66, 905-925.

Wakefield, P. (1816) An Introduction to the Natural History and Classification of Insects in a series of Familiar Letters with Illustrative Engravings. Darton, Harvey & Darton, London.

Walker, P., Leather, S.R. & Crawley, M.J. (2002) Differential rates of invasion in three related alien oak gall wasps (Cynipidae: Hymenoptera). Diversity & Distributions, 8, 335-349.

Weld, L. H. (1926) Field notes on gall-inhabiting cynipid wasps with descriptions of new species. Proceedings of the United States National Museum, 68, 1-131.

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-3032.1940.tb00573.x

https://www.britishplantgallsociety.org/bedeguar-keys.pdf

*

my wife tells me that I am always starting sentences like this and more often than not, it is not interesting at all 🙂

 

Not all moths have wings

Insects really took off when they developed flight (Alexander, 2015), so it is perhaps surprising that so many have lost the ability subsequently.  Nearly all the winged Orders have developed flightless members, with beetles of course, topping the list (Wagner & Liebherr, 1992).  A number of reasons for why flightlessness made a reappearance have been put forward. The eminent coloepterist, Thomas Vernon Wollaston, noted that the island of Madeira had an unusually high number of wingless (apterous) beetles. His friend, Charles Darwin, suggested that for island dwelling animals, it was a disadvantage to be winged especially if you were small or subjected to high winds (Darwin, 1859). Many years later, Derek Roff reviewed the literature, and found that there was no difference in the proportion of non-winged insects on islands compared with those on continental areas (Roff, 1990).  Winglessness is also common in insects living at high altitudes, in cold climates or in those that are autumn or winter active (Hackman, 1966).  It might be that wings are energetically costly in those environments (Mani, 1962), but why then is it that in many cases, it is only the females that are wingless?  To explain this we can hypothesise that eggs are energetically more expensive than sperm (Hayward & Gilooly, 2011), so that males can ‘afford’ to be winged and travel to find a mate. For this to work, the females need to be able to attract males from a distance, something moths are renowned for (Greenfield, 1981).

Male Thyridopteryx ephemeraeformis – note the well-developed antenna – ideal for picking up female sex pheromones. https://upload.wikimedia.org/wikipedia/commons/4/4d/-_0457_%E2%80%93_Thyridopteryx_ephemeraeformis_%E2%80%93_Evergreen_Bagworm_Moth_%2814869905567%29.jpg By Andy Reago & Chrissy McClarren [CC BY 2.0 (http://creativecommons.org/licenses/by/2.0)%5D, via Wikimedia Commons

We also know that in those insects with wing dimorphism, the apterous forms are more fecund compared with those with wings (Dixon, 1972; Mackay & Wellington, 1975). In those insects that retain their wings, many resorb their wing muscles once they have found suitable egg laying sites (Stjernholm et al., 2005; Tan et al., 2010), further proof that wings are costly. Winglessness is also common in those insects that are parasitic on vertebrates, bedbugs, fleas and lice for example.  Those that do start with wings, such as the Hippoboscid flies, lose their wings once they have found a suitable host. Finally, winglessness is often associated with stable and extensive habitats, such as forests, or surprisingly to me at any rate, mountains, where dispersal is not a high priority (Roff, 1990).

Thyridopteryx ephemaeraeformis https://ideastations.org/sites/default/files/storage/secondary-images/bagworm-case.jpg  

I first saw bagworms as a child in Jamaica but of course at the time had no idea what species they were. I was however, fascinated by the sight of the cunningly constructed cases in which the larvae lived and eventually pupated within.  To me, case bearer moths and caddisflies were the insect equivalent of hermit crabs, which were and are one of my favourite non-insect animals*.  Little did I know that one day I would write about these very same bagworms (Rhainds et al., 2008). Bagworms, of which just over half have wingless females, immediately contradict the cold climate hypothesis of winglessness, as many of them are tropical and there are just as many wingless species in the tropics as there are elsewhere (Rhainds et al., 2009). The bagworms belong to the family Pyschidae, which contain a 1000 species or so.  Not only do over half of these have wingless females, some also have females which are legless and never leave their pupal case, even mating in it.

Male Thyridopteryx ephemeraeformis bagworm mating with bag-enclosed female (Jones, 1927)

Even though the more primitive (less derived) members of the Psychidae have wings, the winged females are less active than the males (Rhainds et al. 2009).  As you might expect, host plant selection is by the larval stage, which on hatching, throw out a silk thread and float off with great expectations (Moore & Hanks, 2004).  Once they find a suitable host plant, which is not as difficult as you might expect, as they extremely polygamous, they begin to feed and construct their cases.  Some of the larval cases that Psychids construct are truly magnificent.  A great example is Eumeta crameri, the large faggot worm, so called because it looks like it is carrying a pile of firewood on its back 🙂

Eumeta crameri, the large faggot worm, so called because of the twigs its carries around on its back Melvyn Yeo

In case you are wondering about the ornate cases, they are not decorative, but more likely to be anti-predator devices (Khan, 2020).

Although the Psychids have the largest number of species with wingless females, there are 18 other moth families with species with wingless females.  Species that are found at high altitudes and northern latitudes have the most flightless species (Hackmann, 1966) or, like the Psychids, inhabit stable forest and woodland habitats (Barbosa et al., 1989).  Another characteristic of wingless moth species is that they overwinter as eggs or first instar larvae (Barbosa et al., 1989, although there are of course, many moths that have similar habits and are not wingless, such as the small ermine moths (Leather, 1986a).

After the Psychids, the families with the greatest number of species with wingless females are the Geometridae (loopers) and the Lymantridae (tussock moths). In the Lymantridae some are wingless and many have non-functional wings (Hackman, 1966).  The Arctidae and the Lasiocampidae also have some flightless species, the genus Chondrostega, endemic to the Iberian Peninsula having some notable examples, (Hackman, 1966). An oddity, as they are not strictly flightless, are females of the tortricid Choristoneura fumiferana, which have functional wings, but are behaviourally flightless, only taking flight under particular environmental conditions (Barbosa et al., 1989).

Moth species that have flightless females all have one thing in common, they aren’t picky about their diet, they are polyphagous and live in forests and woodlands. They also tend to have larvae that can disperse by ballooning, although not all moths with ballooning larvae have flightless females.  First instar larvae of the pine beauty moth, Panolis flammea, which readily balloon in outbreak situations, and usefully, can survive several days without food (Leather, 1986b).

In the UK there are two very common moths with wingless females, the winter moth, Operphthera brumata and the Vapourer moth, Orgyia antiqua, the former a Geoemtrid, the latter, a Lymantrid. Both are extremely polyphagous, usually feeding on broadleaf trees and shrubs, but both have recently added conifer species to their diets.  The Vapourer moth ‘decided’ that the introduced lodgepole pine, Pinus contorta growing in Sutherland and Caithness, would make a suitable alternative food plant (Leather, 1986) and the winter moth opted for another introduced conifer, Sitka spruce, Picea sitchensis, in the Scottish Borders (Hunter et al., 1991). Why both these host shifts happened in the early 1980s and in Scotland, remains a mystery, although it is possible that they moved onto conifers via heather (Hewson & Mardon, 1970; Kerslake et al., 1996).

They do, however, have some striking differences in their approach to life. Larvae of the Winter moth are spring flush feeders, and very dependent on egg hatch coinciding with bud burst (Wint, 1983), Vapourers are summer foliage feeders so are adapted to feeding on mature leaves. The adults of the Winter moth, as its name suggests are active in the winter months, laying their eggs on the bark or in crevices of their host trees in November and December and even January. Vapourer adults on the other hand are summer active, the eggs being laid on their pupal cases on the leaves of their host trees from July to September.

Female Vapourer moth and her egg mass – note the short legs and much reduced wings

 

Long legged female winter moth Operphtera brumata https://butterfly-conservation.org/sites/default/files/styles/large/public/2019-01/8179909985_76865dd047_o.jpg

Hackman (1966) distinguishes two types of wingless females, those with reduced locomotion, very heavy, filled with eggs and what I describe in class as splurgers, i.e. all their eggs laid in one go.  The female Vapourer with short legs and much-reduced wings is an ideal example.  The female winter moth is a good example of the second type, those possessing good strong legs which after copulation seek out suitable egg-laying sites.  Despite the difference in oviposition tactics, the first instar larvae of both species are adept ballooners, and it is they who ‘decide’ whether to stay or go (Tikkanen et al., 1999).

First instar Vapourer moth larvae in the process of dispersing.

Understandably, they have very little control of where they land, although presumably, they can reject the plant they land on and launch themselves into space again. How many times they can do this and how long they can live for without feeding, is something that needs research, but given that the first instar larvae of the pine specialist P. flammea can live several days without feeding, I would expect that the Winter moth and Vapourer moth larvae are equally capable of resisting starvation.

Moths without wings, but highly successful and many are pests, so not such a dumb approach to life after all?

And while we’re at it, here is the lymantriid Teia anartoides. With hamsterlike apterous females! AinsleyS @americanbeetles

References

Alexander, D.E. (2015) On the Wing, Oxford University Press. (This is an excellent book).

Barbosa, P., Krischik, V. & Lance, D. (1989) Life history traits of forest-inhabiting flightless lepidoptera. American Midland Naturalist, 122, 262-274.

Darwin, C. (1859) 0n the Origin of Species, JohnMurray, \lodnon.

Dixon, A.F.G. (1972) Fecundity of brachypterus and macropterous alatae in Drepanosiphum dixoni (Callaphididae, Aphididae). Entomologia experimentalis et applicata, 15, 335-340.

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

Hackman, W. (1966) On wing reduction and loss of wings in Lepidoptera. Notulae Entomologicae, 46, 1-16.

Hayward, A. & Gillooly, J.F. (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS One, 6, e16557

Hewson, R. & Mardon, D.K. (1970) Damage to heather moorland by caterpillars of the vapourer moth Orgyia antiqua L. (Lep., Lymantridae). Entomologist’s Monthly Magazine, 106, 82-84.

Hunter, M.D., Watt, A.D. & Docherty, M. (1991) Outbreaks of the winter moth on Sitka spruce are not influenced by nutrient deficiencies of trees. Oecologia, 86, 62-69.

Jones, F.M. (1927) Mating of the Psychidae (Lepidoptera). Transactions of the Entomological Society of America, 53, 293-312.

Kerslake, J.E., Kruuk, L.E.B., Hartley, S.E. & Woodin, S.J. (1996) Winter moth (Operophtera brumata (Lepidoptera: Geometridae)) outbreaks on Scottish  moorlands; effects of host plant and parasitoids on larval survival and development. Bulletin of Entomological Research, 86, 155-164.

Khan, M.K. (2020) Bagworm decorations are an anti-predator structure.  Ecological Entomology https://onlinelibrary.wiley.com/doi/epdf/10.1111/een.12876

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

Leather, S.R. (1986b) The effect of neonatal starvation on the growth, development and survival of larvae of the pine beauty moth Panolis flammea. Oecologia, 71, 90-93.

Leather, S.R. (1986c) Keep an eye out for the vapourer moth. Forestry & British Timber, 15, 13.

Mackay, P.A. & Wellington, W.G. (1975) A comparison of the reproductive patterns of apterous and alate virginoparous Acyrthosiphon pisum (Homoptera: Aphididae). Canadian Entomologist, 107, 1161-166.

Mani, M.S. (1962) Introduction to High Altitude Entomology: Insect Life above the Timber-line in the Northwest Himalaya. Methuen, London.

Moore, R.G. & Hanks, L.M. (2004) Aerial dispersal and host plant selection by neonate Thyridopteryx ephemeraeformis (Lepidoptera: Psychidae). Ecological Entomology, 29, 327-335.

Rhainds, M., Leather, S.R. & Sadoff, C. (2008) Polyphagy, flightlessness and reproductive output of females: a case study with bagworms (Lepidoptera: Psychidae). Ecological Entomology, 33, 663-672.

Rhains, M., Davis, D.R. & Price, P.W.(2009) Bionomics of Bagworms (Lepidoptera: Psychidae). Annual Review of Entomology, 54, 209-226.

Roff, D.A. (1990) The evolution of flightlessness in insects. Ecological Monographs, 60, 389-422.

Stjernholm, F., Karlsson, B. & Boggs, C.A. (2005) Age-related changes in thoracic mass: possible reallocation of resources to reproduction in butterflies. Biological Journal of the Linnean Society, 86, 363-380.

Tan, J.Y., Wainhouse, D.W., Day, K.R. & Morgan, G. (2010) Flight ability and reproductive development in newly-emerged pine weevil Hylobius abietis and the potential effects of climate change. Agricultural and Forest Entomology, 12, 427-434.

Tikkanen, O.P., Carr, T.G. & Roininen, H. (1999) Factors influencing the distribution of a generalist spring-feeding moth, Operophtera brumata (Lepidoptera: Geometridae), on host plants. Environmental Entomology, 28, 461-469.

Wagner, D.L. & Liebherr, J.K. (1992) Flightlessness in insects. Trends in Evolution & Ecology, 7, 216-219.

Watt, A.D., Evans, R. & Varley, T. (1992) The egg-laying behaviour of a native insect, the winter moth Operophtera brumata (L.) (Lep., Geometridae), on an introduced tree species, Sitka spruce, Picea sitchensis. Journal of Applied Entomology, 114, 1-4.

Wint, W. (1983) The role of alternative host-plant species in the life of a polyphagous moth, Operophtera brumata (Lepidoptera, Geomtridae). Journal of Animal Ecology, 52, 439-450.

Wollaston, T.V. (1854) Insecta Maderensia, John van Voorst, London.

 

*although I also have a very soft spot for pseudoscorpions