The spider and the tuning-fork

Having started to look at identification of spiders, I've been meaning to buy a tuning-fork for some time, and last week I finally remembered to go into a music shop and get one. 'What has a tuning-fork got to do with spiders?' you may ask. Well, for quite some time, it's been known that spiders detect vibrations from their prey, such as insects caught in their webs and from the exact strands that are vibrating know where on the web their potential prey is located. They don't respond to slower taps on their webs as these are far too low a frequency and might be a larger predator hunting them instead. So, if you get a vibrating tuning-fork and touch an occupied spider web, there's a fair chance that the spider will emerge, lured out by the fake meal. Just watch...

I haven't identified the spider, but it looks like one of the several similar species of Tegenaria that inhabit such places - houses, outbuildings, and (as in this case), garden sheds. You can see that it emerges when the vibrating fork touches the web, and immediately attacks the 'prey' (suggesting that vision is less important at this point) - when the fork is removed, the spider returns to its funnel-shaped retreat. This is a good example of this 'trick', but things are rarely as simple as they seem, so what's going on from a biological perspective?

It was way back in the late 19th century when the 'influence of a tuning-fork on the garden spider' was first (as far I am aware) scientifically reported (Boys, 1880). Since then, a considerable amount of research has been undertaken. For example, Parry (1965) investigated the signal that a prey insect generates, noting that previous work had tended to focus on artificial signals similar to the sinusoidal wave generated by a tuning-fork. Tretzel (1961) had already found that prey made higher frequency sounds with a greater range of intensities than young spiders (which were therefore lower-pitched and more even) but was uncertain whether spiders used frequency to differentiate between prey and their own young, though they clearly can differentiate between them in some way; similarly at this time there was a lack of evidence about how spiders differentiated between prey and inanimate objects hitting the web. Taking a more straightforwardly visual approach, Savory (1952) had observed responses of Tegenaria to tuning-forks and found that:

• The spider first runs to the fork and try to grasp and bite it (as seen in the video).
• If the fork is used repeatedly, the attack reponse ceases as if the spider has learned there is no prey ( I found that the spider in my video only responded twice - the third time it stayed in its retreat).
• However, if a fork with a different vibration frequency is used, the attack reponse starts again (if it were a prey insect, there would be a complex range of frequencies of vibration).

Conveniently given the subject of my video, Parry also looked at Tegenaria and found segments of sound that he termed 'fast transients' - essentially parts of the prey insect (legs, antennae) 'plucking' web threads like a guitar string, either by dragging across them or by becoming detached and allowing the thread to snap back into position.

As the spider grips a bundle of threads in the claws of its front legs, these 'plucks', along with high-frequency vibrations are easily transmitted to it from the web. Little more could be concluded but Walcott (1969) investigated the structure of the sensitive receptors on the 'feet' of all eight legs of the house spider Achaearanea tepidariorum. He found a lyriform ('lyre-shaped') sense receptor organ with 10 receptor units, each sharply tuned to particular frequencies between 60 and 1400 Hz, although the sensitivity of each  unit depended on the tension of the slits forming the organ (think of it as a 'harp' or 'guitar'-like arrangement). However, it was responsive to air-borne vibrations, not web-borne ones, presumably because the web of this species was a poor transmitter. This arrangement also implies that the 'learning' response that prevents repeated attacks on a fake prey stimulus (if the same frequency of fork is used) is linked to one or a few units being effectively switched off for a period). Later research by Barth & Geethabali (1982) investigated the function of the lyriform organ in more detail and concluded that the units/slits were not tuned to particular frequencies but that there was some difference in the precise response curves that could allow frequency discrimination; they also concluded that vibration sensing was only one function of the lyriform organ and that it might also be involved in proprioception (i.e. the spider's own sense of where its limbs are, just as you know where your arms and legs are when you have your eyes shut). This contradicts Walcott (1969) but this may of course be due to genuine differences between spider species.

Now, I could go on - and indeed much has been written on this subject, but it turns out that the range of responses is highly variable. Different species of spider focus on different frequencies (or ranges of frequency with differing response intensities); the extent to which visual cues are used varies (e.g. in the ogre-faced spiders Deinopsis, the simple eyes are large in order to hunt at night, while some species have reduced eyes), as does the response e.g. the 'attack' seen in the video is common, but a 440 Hz fork (as used above) has been reported as causing the orb-weaver Eriophora sagana to fall from its web in a predator-avoidance response rather than treating the vibrations as prey (e.g. Nakata 2008). This work has indicated that airborne vibrations are used by E. sagana to detect insect predators, and that predation can lead to changes in web structure - thus there is a complex interaction between prey availability (in the sense of web structure being related to prey capture) and predation risk, with vibration detection being a mechanism that at least partly informs this balance.

The upshot of this? Well, first of all there is clearly more to be understood, even with a simple experimental tool such as a tuning-fork. I certainly intend to look at the responses of other spiders such as orb-weavers and jumping spiders. Secondly, I might have to buy a wider range of tuning-forks. Thirdly, if you've tried this, please do leave a comment to say what happened.

References

Barth, F.G. & Geethabali (1982). Spider vibration receptors: Threshold curves of individual slits in the metatarsal lyriform organ. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 148(2): 175-185.

Boys, C.V. (1880). The influence of a tuning-fork on the garden spider. Nature 23: 149-150.
Nakata, K. (2008). Spiders use airborne cues to respond to flying insect predators by building orb-webs with fewer silk threads and larger silk decorations. Ethology 114: 686-692.
Parry, D.A. (1965). The signal generated by an insect in a spider's web. Journal of Experimental Biology 43: 185-192.
Savory, T.H. (1952). The Spider's Web. Warne, London.
Tretzel, E. (1961). Biologie, Okologie und Brutpflege von Coelotes terrestris (Wider) (Araneae, Agelenidae). Teil II : Brutpflege. Z. Morph. Okol. Tiere 50: 375-542.
Walcott, C. (1969). A spider's vibration receptor: its anatomy and physiology. Amer. Zool. 9(1): 133-144.

Birds in a box, beetles on pins

For those involved directly in taxonomy and species identification, the function of biological collections is well known e.g. to provide reference specimens, and more recently to create a potential source of genetic material for molecular research. For others, it may seem a somewhat outdated, even macabre, activity, but this is not the case as long as ethical guidelines are followed - such as a 'code of conduct for collecting' (there may also be legislation covering collecting that varies from country to country, so do beware and check for protected species and permit requirements). During my recent visit to the Oxford University Museum of Natural History (which I've heard referred to rather dismissively as 'the dead animal building'), I came across two excellent examples of why biological collections are of key importance in life science research. The first is an area you may have noticed me writing about quite a lot - small beetles; the second is quite different but more widely familiar, at least in broad terms.

A tray of scarabaeid beetles from the Hope Entomological Collections at the OUMNH

Trays of insects on cards and/or pins is one popular perception of a biological collection, along with stuffed animals, skeletons and 'pickled things in jars'. Although this is no some extent rue (visually at least), their purpose is not always well understood. For example, one reason for my recent visit to the OUMNH was to consult the Hope Entomological Collections. With over 5 million specimens this is the second most important such collection in the UK after that at the Natural History Museum in London. My reason for wanting to consult the collection was to help finish my key to identifying British Chrysomelidae, in particular the last few tricky species of Longitarsus flea beetles - L. curtus, L. fowleri and L. membranaceus. These are superficially very similar and I wanted to check some characteristics so that I could decide how to separate them in my book. They are also tricky because (a) I don't have my own beetle collection (I have nowhere to store one), (b) there is a very good collection maintained by the Hampshire Museums Service in Winchester; however although it is only 10km away, it tends to only be open when I am at work (an increasing problem in the UK as local government funding cuts reduce staffing and thus opening hours), and (c) these three species are not available as clear online photographs, even at the excellent European Chrysomelidae website. So, I went to Oxford to have a look at theirs - in particular fine details of the heads.

Longitarsus membranaceus

Longitarsus curtus

Longitarsus fowleri

I won't go into great morphological detail here, but the result is that I can now tell these three species apart from details of their heads - and so will anyone else be able to once my key is published - but in summary, L. membranaceus has a distinctive broad bar running down the front of its head, the sides of the bar being more or less parallel where it runs between the upper halves of the eyes, and it has a narrow process extending down between the antennal bases. In L. curtus, there is a broad wedge rather than a bar and this meets the upper edges of the eyes. In L. fowleri, the bar broadens towards the top of the head but is still separate from the eyes. So, with specimens and a microscope, a fairly straightforward way to separate some very similar species without needing to dissect them - and one that does not appear in existing keys, but could not have been determined without access to a collection. Plus, as I remembered to take my camera, there are now some useful photos that will appear when these species are Googled! Now, moving on to the second example, I enter the realm of an iconic vertebrate, the dodo (Raphus cucullatus).

The Oxford dodo display

This was not something I specifically went to visit, though it is an important exhibit, not just because the dodo is a popular metaphor for extinction, but because of the the information that can be gained by having the specimen in a biological collection. It is well known that the dodo was first discovered by Europeans on Mauritius in 1598 and that it was extinct by 1680 (though probably due more to pressure from other introduced animals rather than hunting by humans - apparently it wasn't very tasty!). However, despite being so iconic, little was known about its biology and ecology until recently. The best-known contemporary images are 17th and 18th century paintings but their portrayals of fat dodos are now known to be inaccurate, with research since the 1990s indicating a much slimmer bird even if precise estimates differ and work is ongoing (Kitchener, 1993a, b; Angst et al., 2011). The importance of the OUMNH's dodo specimen lies in the fact that it is the only specimen in the world with soft tissue preserved (skin on the head) from which DNA could be extracted. When this was analysed, the dodo, and its close relative the solitaire Pezophaps solitaria from the (relatively) nearby Rodrigues island, were found to be most closely related to the pigeons within the family Columbidae (Shapiro et al., 2002). This is a key result as the dodo had previously been taxonomically linked not just to pigeons, but also parrots, shorebirds and raptors - partly due to the lack of evidence/specimens and partly because of the considerable amount of adaptation and specialisation that occurred in its island location that rendered it superficially unlike any other bird, apart from the similarly poorly understood solitaire. The research indicates that the dodo and solitaire separated from south-east Asian relatives around 40 mya while able to fly, and dispersed to the Mascarene Islands. The dodo and solitaire then separated around 26 mya; Mauritous and Rodrigues are much younger (only around 8 and 1.5 my old respectively) which implies that the birds used the now-sunken Mascarene island chain as stepping stones, with the isolation of Rodrigues implying that the solitaire was able to fly as recently as 1.5 mya.

So, although genetics is only one area of research, and like any other needs to be applied and interpreted appropriately, this is an example where a modern technique and a traditional biological collection were both required for research purposes and combined to produce important results - the dodo is much more than a stuffed bird in a case, and genetics needs real-world applications beyond 'bar-coding' of species. It also highlights the point that when a specimen is collected, its use may be unknown as this specimens dates from long before the concept of the gene had been thought of. For an overview of some other applications of this technology, Nicholls (2005) covers some important points, and for much more detail about the 'Oxford dodo', have a look at this excellent OUMNH factsheet which I mercilessly plundered for background information.

References

Angst, D., Buffetaut, E. & Abourachid, A. (2011). The end of the fat dodo? A new mass estimate for Raphus cucullatus. Naturwissenschaften 98(3): 233-236.

Kitchener, A.C. (1993a). On the external appearance of the Dodo Raphus cucullatus (L.). Archives of Natural History 20(2): 279-301.

Kitchener, A.C. (1993b). Justice at last for the Dodo. New Scientist. (28.8.93)

Nicholls, H. (2005). Ancient DNA Comes of Age. Public Library of Science Biology 3(2): e56

Shapiro, B., Sibthorpe, D., Rambaut,A., Austin, J., Wragg, G.M., Bininda-Emonds, O.R.P., Lee, P.L.M. & Cooper, A. (2002). Flight of the Dodo. Science 295: 1683.

Circus of the Spineless #68 - gifts galore!

It's December, so it's tempting to come up with a festive theme for this edition of Circus of the Spineless. However, I'm going for a 'birthday' theme instead because it's my blog's 'official' 1st birthday - 'official' (like the Queen's) because it's about a year since it really got going though I started it a bit before that. And, my 20,000th pageview just appeared, so thanks to whoever that was! Anyhow, I digress - please do click to take a giftbox, a slice of virtual cake and/or a glass of whatever suits you...

First up, Susannah of Wanderin' Weeta fame has provided some gift-wrapped goodies found tucked away in a vacant lot ('brownfield site' in UK-speak!) which goes to show it's always worth a look. To celebrate, why not start with a slice of tasty cake...

Next, a pair of splendid parcels arrived from John at 'Carp Without Cars' - the first arrived as 'snail mail' but not really (you'll see what I mean, just drink from the glass of finest red) and the second comes in a smaller package that rarely displays its contents quite as clearly as this...

My birthday cup already runneth over, but there's more to come... Here, Daniel at 'Notes from Dreamworlds' takes a close, close look at some freshwater critters courtesy of some high-quality optics (feel free to contrast this with the microscopy efforts on my blog!) and wraps the whole thing up as an 8-minute video - a veritable treasure-chest of precious things.

And lastly, I shall give myself a small gift of shameless self-promotion... Here, I look at the shiny jewelled contents of a box that really did turn up in the mail, so why not sit back with an ice-cold beer - mmm.... foamy...

So, that's all from my birthday-themed CoS #68 - thanks for coming along to the party; the more the merrier and there's no-one on the door to check for invitations. Next month, prepare yourself for some myrmecology as CoS scuttles off to Wild About Ants. Byeeee.

Ecologist + shed = home-made canopy sampler

Today, it's time to move away from obscure invertebrates and have a look at the kit I use to find some of these things - not the usual pooters, beating trays and nets, but something a little more unusual.

I do quite a lot of invertebrate-hunting in all sorts of habitats - grasslands, heathlands, woodlands, coastal areas and so on. Of these, one is particularly tricky - woodland. At ground level it's fine, but I can't help but wonder what's up in the canopy that I can't get at - certainly there's a lot of recent research into canopy ecology around the world (e.g. here) following realisation of its importance alongside some technical advances aiding the research work itself. On a large scale and/or with lots of funding, there are various options - smoking whole trees, building canopy walkways, laying flexible platforms across the treetops, and so on. On a smaller and cheaper scale, there is the option of hoisting flight interception traps into treetops and leaving them to see what falls in before returning to collect the catch. This is something I can do, but a lot of my surveys involve a limited number of visits quite widely separated. This means that traps would have to be left for too long and might suffer from interference from members of the public (unless tied off further up the trees, but that means climbing). So, I got to thinking about how to sample the canopy whilst actually on site and without having to get roped and harnessed.

This meant being able to get a sampling device in and out of the canopy at will, and that the device had to be sufficiently portable to carry by hand from the nearest access point (which can be some distance away). Although tempted by something involving a remote-control helicopter, this seemed fraught with dangers of both cost and getting it stuck up a tree. Nope, that idea was quickly scrapped in favour of something else - a lightweight telescopic pole with a canopy sampler on the end. So, how does that work..?

First, get a series of aluminium poles and cut/fit them as follows:

A set of aluminium poles, three of which have a short section of narrower pole riveted into one end so that they are interlocking. Drill holes through so that they can be fitted together and held in place with wing-nuts. The fourth one has a hook at the end to catch and shake branches and can also be bolted into place. If you think your drilling may vary a bit between poles, which would mean they have to fit in a particular order, number your first three poles 1-3...

Short section riveted into large section

Wing-nut fixing in situ

Hooked end on pole four. A wire hangs from the bend with one or more loops (to adjust the height of the sampler) at the end. This could equally be strong cord or any other suitable material.

That's the pole arrangement, but what about the sampler? This requires an inverted truncated cone open at both ends with a smooth inner surface (try an unwanted lampshade). This has a long thin bag (fine mesh; the one below was made from net curtain) sewn onto the smaller hole and strings for suspension (via a carabiner or similar clip) attached over the larger hole.

Sampler consisting of bag, cone, strings and carabiner modelled by our washing line...

This is clipped onto looped wire and the whole thing hoisted up into a tree canopy - the hook is then used to shake branches, dislodging invertebrates which then helpfully fall into the cone and slide into the mesh bag.

The sampler in action, modestly extended, and modelled lovingly by me in our back garden...

So, onto the main question - does it work? Well, I have tried it on a number of surveys and the answer is yes. The whole arrangement is 4+ metres long so with the user's height/reach means that it can sample up to about 6 metres above the ground. Although some specimens undoubtedly escape as with nets and beating trays, each use has provided species which had been missed by sampling directly below at ground level. I have yet to undertake a rigorous study but hope to find some time to quantify exactly which groups it is best for, although initial indications are that weevils are one group readily captured. I'm also hoping to find that some under-recorded canopy-dwelling groups and species are readily caught, but only time (and sampling/identification effort) will tell, so watch this space!