Not all aphids take the same risks

In 1970 an entomologist working on the black bean aphid, Aphis fabae, at Rothamsted Experimental Station (as it then was),  noted that he could categorise the winged individuals as either migrants, flyers or non-flyers; the former flying before they reproduced, the second flying after they reproduced and the final category, never flying (Shaw, 1970).  To describe this phenomenon he used the phrase “migratory urge” a term previously only used in the ornithological literature.

A few years later a group of PhD students in Tony Dixon’s lab at the University of East Anglia started dissecting aphids and counting their ovarioles, finding that unlike most other insects, ovariole number was variable within a species and not related to adult weight (Dixon & Dharma, 1980; Wellings et al., 1980; Leather, 1983).  Generally speaking, in insects, including aphids, the heavier they are, the more fecund they are, although in some instances this is not always true (Leather, 1988).

Figure 1 taken from http://www.aphidsonworldsplants.info/Cloning_Experts_3.htm

Figure 2 What aphid ovarioles really look like Dombrovsky  et al. BMC Research Notes 2009 2:185   doi:10.1186/1756-0500-2-185

What we found then (Wellings et al., 1980), and later (Leather et al., 1988), was that aphids with wings (alatae) even those from the same clone, had much more variability in the number of ovarioles contained within them than those without wings (apterae) (Leather et al., 1988), and that the more ovarioles an aphid contained the more fecund it was, although as mentioned earlier the number of ovarioles appeared to be independent of weight (Leather & Wellings, 1981).

So what does this have to do with migratory urge in Aphis fabae? In the early 1980s Keith Walters was working on migration in cereal aphids (Sitobion avenae and Rhopalosiphum padi) and discovered, that as with Aphis fabae these two species also produced alatae with different flight attributes (Walters & Dixon, 1983).  Building on what we in our group had discovered about ovarioles, Keith was able to show that the degree of migratory urge in aphids was determined by the number of ovarioles they contained. The greater the number of ovarioles the more reluctant they were to take flight (Figure 3ab).

Figure 3a Relationship between number of ovarioles and time to take-off (minutes) in Sitobion avenae  (Drawn from data in Walters & Dixon, 1983).

Figure 3b Relationship between number of ovarioles and time to take-off (minutes) in Rhopaloisphum padi  (Drawn from data in Walters & Dixon, 1983).

 He also found that the fewer the number of ovarioles, the steeper the angle of take-off was (Figure 4) i.e. aphids with few ovarioles climbed faster and more steeply and were thus more likely to end  up higher in the air, and thus more likely to travel further than those

Figure 4 Relationship between number of ovarioles and angle of take-off (degrees) in Rhopalosiphum padi (drawn from data in Walters & Dixon, 1983).

taking off at a shallower angle.  He also showed that resistance to starvation was greater in those aphids with fewer ovarioles and that they could also fly for longer periods of time.  Given that alatae of Aphis fabae also have a variable number of ovarioles, 6-12 (Leather et al., 1988), we can see that this fits in very well with Shaw’s classification of migrants, flyers and non-flyers.

This is yet another great example of the flexibility (plasticity) of the aphid clone.  By producing offspring that have different flight capabilities and propensities, the clone is able to hedge its bets in times of adversity; alate aphids in many aphid species are produced in response to crowding and/or poor nutritional quality (Dixon, 1973).  This deterioration in living conditions could be very local i.e. restricted to the plant on which the aphid is feeding or its immediate neighbours, slightly more widespread, i.e. at a field scale or at a much more widespread landscape scale.  Given that long distance aphid migration is very costly (only a tiny proportion survive, Ward et al, 1998) the best option is to spread the risk between the members of your clone.  Those individuals with more ovarioles and greater potential fecundity make the low risk short-distance hops (trivial flights), but take the chance that the next door plant might be just as bad as the one left behind and also within easy reach of natural enemies, but with a higher chance of arriving and reproducing.

A risk taking aphid!

 

At the other end of the scale, those clone members with fewer ovarioles and reduced potential fecundity make the long distance migratory flights, with the risk of not finding a suitable host plant in time, but with the chance that if they do, it will be highly nutritious and natural enemy-free.  A really good example of not putting all your eggs in one basket and yet again a demonstration of what fantastic insects aphids are 😉

 

References

Dixon, A.F.G. (1973) Biology of Aphids Edward Arnold, London.

Dixon, A.F.G. & Dharma, T.R. (1980) Number of ovarioles and fecundity in the black bean aphid, Aphis fabae. Entomologia Experimentalis et Applicata, 28, 1-14.

Leather, S.R. (1983) Evidence of ovulation after adult moult in the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia experimentalis et applicata, 33, 348-349.

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

Leather, S.R. & Welllings, P.W. (1981) Ovariole number and fecundity in aphids. Entomologia experimentalis et applicata, 30, 128-133.

Leather, S.R., Wellings, P.W., & Walters, K.F.A. (1988) Variation in ovariole number within the Aphidoidea. Journal of Natural History, 22, 381-393.

Shaw, M.J.P. (1970) Effects of population density on the alienicolae of Aphis fabae Scop.II The effects of crowding on the expression of migratory urge among alatae in the laboratory. Annals of Applied Biology, 65, 197-203.

Walters, K.F.A. & Dixon, A.F.G. (1983) Migratory urge and reproductive investment in aphids: variation within clones. Oecologia, 58, 70-75.

Ward, S.A., Leather, S.R., Pickup, J., & Harrington, R. (1998) Mortality during dispersal and the cost of host-specificity in parasites: how many aphids find hosts? Journal of Animal Ecology, 67, 763-773.

Wellings, P.W., Leather , S.R., & Dixon, A.F.G. (1980) Seasonal variation in reproductive potential: a programmed feature of aphid life cycles. Journal of Animal Ecology, 49, 975-985.

 

Entomological classics – the pitfall trap

 I would be amazed if there are any entomologists who have not deployed a pitfall trap or two at some stage in their career. I would also hazard a guess that quite a few non-entomological ecologists have come across the joys of pitfall trap setting and catch sorting as part of their undergraduate training; most field courses seem to include a pitfall trap day, and rightly so.  Pitfall trapping is after all, probably the simplest and most efficient way of collecting data, and not always insects 😉

Tapir pitfall trap

More seriously though, pitfall traps are a remarkably simple and incredibly versatile way of sampling insects, particularly those that are active on the soil surface (epigeal) e.g carabid beetles. They can be used in most habitats where you are able to dig into the soil,

are very cheap as they can be made from easily obtainable household materials  and can be modified easily depending on your objectives and sampling conditions.  It is very important however, that the lip of the trap is either flush with or below the soil surface.  Not very many beetles or other invertebrates,  are willing to climb up the steep sides  to allow you to capture them. They are also amenable to being deployed in a variety of statistically meaningful ways. (Figure ‘borrowed’ from Woodcock (2005)). They are of course not perfect.   Some of my students complain that they catch too much!

There has been, and continues to be, much debate about what the catch actually represents.  Are they a measure of activity or of density, i.e. do the trap catches represent the most active and careless beetles, rather than the most abundant?  Southwood (1966) in the first edition of Ecological Methods is fairly dismissive of their use except as a way of studying the activity, seasonal incidence and dispersion of single species and considered them to be of no use whatsoever in comparing communities.  Other authors argue however, that if the trapping is carried out over a long period of time then the data collected can be representative of actual abundance (e.g. Gist & Crossley, 1973; Baars, 1979) and despite Southwood’s comments, they are probably most often used to compare communities (e.g. Rich et al., 2013; Zmihorski et al., 2013;  Wang et al., 2014) For a very thorough account of the use and abuse of pitfall traps see Ben Woodcock’s excellent 2005 article (and I am not just saying that because he is one of my former students). You might expect, given the fact that pitfalls were used by our remote ancestors to trap their vertebrate prey, that entomologists would have adopted this method of trapping very early on, especially given the fact that nature got there first, e.g. as used by larvae of the antlion.

Antlion ‘pitfall traps’.

I was therefore surprised when I started researching this article to find that the earliest reference I could find in the scientific literature was Barber (1931).  I found this very hard to believe so resorted to Twitter.  Richard Jones suggested that a sentence in

Notes on Collecting and Preserving Natural History Objects

referring to silver sand pits might be a reference to an early form of pitfall trap.  On further research however, it turned out that sand pits were the results of sand mining operations and were used opportunistically by entomologists.  They worked in a very similar way to

St Austell Ruddle Moor Sand Pit http://www.cornwall-opc.org/Par_new/a_d/austell_st.php

intercept traps (the subject of a future post).   Interestingly, in some parts of the world, sand pits are now being restored in some places as conservation tools for digger wasp sand bees.

Sand pit restoration – Bohemia.  http://www.outdoorconservation.eu/project-detail.cfm?projectid=17

  But, I digress.  My next port of call was The Insect Hunter’s Companion (Greene, 1880) which I felt certain would mention pitfall traps.  To my surprise, in the 1880s, entomologists intent on capturing beetles, either pursued them with nets, turned over stones and logs, removed bark from trees, used beating trays or even dug holes in the ground, but never used pitfall traps!  So all very active and energetic methods – no sit and wait in those days 😉 So it seems that Barber’s 1931 description of a pitfall trap does indeed commemorate the first scientific use of a pitfall trap.

The Barber trap (Barber, 1931).

Despite their late addition to the entomological armoury and despite the many criticisms levelled at their use, they continue to be perhaps the most widely used method of insect sampling ever; for example if you enter Beetle* AND pitfall* AND trap*  into the Web of Science you will return 1168 hits since 2000, which is more than one a week.  If you further refine your search to exclude beetle but add insect* you can add another 320 hits. If by some chance you have never used a pitfall trap, then I heartily recommend that you set one or two up in a convenient flower bed or even your lawn, and then sit back and wait and see what exciting beasties are roaming your garden.

Post script

Since this post was published I have discovered an earlier reference to the use of pitfall traps (Hertz, 1927).  Many thanks to Jari Niemelä  of Helsinki University for sending me a copy of the reference and many thanks to my eldest daughter for translating the relevant bit, which follows –  “The traps were made of meticulously cleaned tin cans (the rectangle ones used for e.g.  sardines) dug into the ground so deep that the top of the tin was absolutely level with the ground…… it is an ideal way to catch the beetles; with their careless way of running around, they easily fell into the deathtraps, and had no time to use their wings (if they have any)”.  The phrase deathtraps is particularly fine.  The majority of the paper is about the species he caught in different locations and he highlights the fact that he caught seven very rare species using this method.

So this is now the oldest known reference to the use of pitfall traps in the literature, although he does mention that he was using this method to catch beetles in 1914.  But if anyone comes across an earlier reference do let me know.

 

References

Baars, M.A. (1979) Catches in pitfall traps in relation to mean densities of carabid beetles. Oecologia, 41, 25-46.

Barber, H.S. (1931) Traps for cave inhabiting insects.  Journal of the Elisha Mitchell Scientific Society, 46, 259-266.

Gist, C.S. & Crossley, J.D.A. (1973) A method for quantifying pitfall traps.  Environmental Entomology, 2, 951-952.

Greene, J. (1880) The Insect Hunter’s Companion: Being Instructions for Collecting and Describing Butterflies, Moths, Beetles, Bees, Flies, Etc.  

Hertz, M. (1927) Huomioita petokuoriaisten olinpaikoista.  Luonnon Ystävä, 31, 218-222

Rich, M.C., Gough, L., & Boelman, N.T. (2013) Arctic arthropod assemblages in habitats of differing shrub dominance. Ecography, 36, 994-1003.

Southwood, T.R.E. (1966) Ecological Methods, Chapman & Hall, London.

Wang, X.P., Müller, J., An, L., Ji, L., Liu, Y., Wang, X., & Hao, Z. (2014) Intra-annual variations in abundance and speceis composition of carabid beetles in a temperate forest in Northeast China. Journal of Insect Conservation, 18, 85-98.

Woodcock, B.A. (2005) Pitfall trapping in ecological studies.  Pp 37-57 [In] Insect Sampling in Forest Ecosystems, ed S.R. Leather, Blackwell Publishing, Oxford.

Zmihorski, M., Sienkiewicz, P., & Tryjanowski, P. (2013) Neverending story: a lesson in using sampling efficieny methods with ground beetles. Journal of Insect Conservation, 17, 333-337.

 

Post post script

Pitfall traps are even more versatile than you might think. Mark Telfer has developed a nifty subterranean version http://markgtelfer.co.uk/beetles/techniques-for-studying-beetles/subterranean-pitfall-traps-for-beetles/  and at the opposite end of the spectrum, pitfall traps have also been used in trees to sample spiders (Pinzon & Spence, 2008).

Reference Pinzon, J. & Spence, J. (2008) Performance of two arboreal pitfall trap designs in sampling cursorial spiders from tree trunks.  Journal of Arachnology, 36, 280-286

 

Post post script And for those of you who have had to suffer sitting through the Pokémon movie as I did many years ago, there is also a Pokémon version of the antlion!

http://bulbapedia.bulbagarden.net/wiki/Trapinch_(Pok%C3%A9mon)

 and don’t forget Winnie the Pooh and his heffalump trap 😉  Hopefully you will use them more carefully than he did.

Celebrating being 60 by walking the Yorkshire Coast – a pictorial record

Those who follow my blog will remember that I turned 60 on March 13^th and was pleasantly surprised at lunch time by colleagues, students and friends.

There was however, also another treat in store for me.  My best friend from school (John Pearson) and I used to go walking and camping together in our school and university holidays.

Me and John – 21^st Birthday Party

 

Family and jobs put an end to this tradition although we and our wives used to (and still do) get together for short walks and visits.  For our 50^th birthday however, we diced that it was time to get our walking boots back on in earnest and as good Yorkshiremen we decided that we would walk the Yorkshire Coast (or at least part of it).  In the end we enjoyed a very enjoyable walk from Redcar down to Robin Hood’s Bay, as traditional Yorkshiremen, Redcar, despite boundary changes is still Yorkshire territory as far as we are concerned 😉

 

We stayed in pubs and B&Bs along the way, our camping days being long over.  As a point of honour we walked to the end of every pier (and back) on the way down.

For our 60^th birthday, John’s wife Christine paid for three nights in a hotel in Scarborough on the Esplanade for us, The Weston, and we set off to do Robin Hood’s Bay to Bridlington in three days.

The weather forecast was truly awful so we were a bit worried, and certainly driving to Scarboroug on Saturday morning, the weather was not promising.  By lunchtime however, the rain had stopped and apart from a short shower we had remarkably good weather for the end of March.  The last two days were, however extremely windy. Each day, we left a car at our finishing point and drove the other car to our start point; that way we were able to stay in comfort in one location and enjoy a well-earned beer at the end of each day and a bottle of very reasonably priced wine at dinner.  Bliss.

 

Day 1 Robin Hood’s Bay to Cloughton

A gentle start as we only had half a day and wanted to break our feet in gently.  Daffodil and Primula garden escapes were very much in evidence on the cliff sides – actually they were present all the way along the coast.

 

Staring with a beer – Theakstons Black Bull Bitter

Yorkshire at its best

A steep bit (one of many)

View from hotel bedroom – evening

Day 2 – Cloughton to Filey

There were some more very steep bits, but despite the gloomy start, it was mainly nice and sunny.  Insects were not much in evidence, but skylarks were very noticeable, and of course there were lots of sea birds.

First morning – gloomy view from hotel window, but luckily the weather improved as the day progressed.

There were indeed some steep bits,

and some very steep bits as well.

Not forgetting the slippy bits!

Distant objective.

Dramatic cliffs.

Clearing skies – great views.

Day 3 Filey to Bridlington

An extremely windy day, most of the time we felt like we were walking uphill despite a lot of it being on the flat, on the plus side it was quite sunny.

Sunrise – a beautiful start to the day

Not just us that was windswept!

Bempton – lots of Gannets and Guillemots

This was the only puffin we saw!

 

The sea, the sea!

The beach was a bit of a struggle.

Flamborough Head – we came here for our 3^rd form Geography field trip in 1969 – it was joined to the coast then and was a blowhole!

You can’t have a coastal walk without a lighthouse!

Day 4 – Spurn Point

Drove here from Scarborough just to see it as we didn’t feel like slogging along the beach at Bridlington and this is our proposed finishing point for our 65^th birthday walk.  We decided that waiting until we were 70 might not be wise 😉

Clear(ish) skies but gale force winds.

Just like walking in a desert sand storm – we had to turn back after a mile.

The sea was brown not blue! Hopefully when we reach this point in 2020 the wind will have abated!

And just to finish a great piece of seaside sculpture.

Freddie Gilroy on the front at Scarborough.