Antscape: ghosts in the graveyard

Despite the title, it's early March and so couldn't be much further from Halloween, but wildlife respects its own calendar, not ours... Anyhow, having gone for a wander in the woods a few days ago, I took my usual shortcut through the nearby churchyard and noticed something intriguing. On many of the graves, especially on the corner-stones, tussocks of soil and grass had developed. I must have seen this dozens of times before but it had never really grabbed my attention - this time however, I stopped to take a closer look...

Tussocks on the corners of a grave.

From a distance, these tussocks just look like long grass that the mower has missed. However, close up it is clear that they are actually formed of fairly loose soil with grass and moss growing on it. Like any good ecologist, I began to delve...

Yellow Meadow Ants (Lasius flavus) in a churchyard 'tussock'

As soon as pulled open one of these tussocks, it was clear how they had formed - they are actually anthills of the Yellow Meadow Ant (Lasius flavus). L. flavus is a common species, associated with the formation of 'antscapes' comprised of hundreds of closely spaced anthills on undisturbed grasslands (although sometimes they don't form anthills). In Britain it is the only species building long-term nests of the 'unthatched mound' type - a couple of others such as L. niger produce occasional small, temporary mounds, while the Wood Ant Formica rufa produces much bigger mounds covered ('thatched') with bits of twig etc. (Skinner & Allen 1996). L. flavus nests are up to about 30 cm tall, the mound effectively being the spoil heap from soil dug out when the colony builds its underground nest of tunnels and chambers. Being subterranean, L. flavus is rarely seen unless sought out, despite probably being Britain's commonest ant - the underground habit has led to reduced eye development and even soil is brought to the surface at night (Pontin 2005), so daytime activity is unlikely to be seen in passing - certainly I saw no ants on the surface. This also keeps different species apart - in this case, L. flavus lives in the same areas as L. niger, but the latter lives on the surface forming much larger territories (active L. flavus mounds can be as little as 2 m apart, below which inter-colony competition is too intense and queens are attacked prior to establishment of a new colony) (Pontin 2005). As the ants cannot make mounds in mowed (or heavily grazed) areas, it is clear that their use of the graves as a focus for their anthills allows them to avoid disturbance by mowers. In meadows, I have seen newly forming nests being built around plant stems - possibly to provide an initial scaffolding for the loose soil particles.

Like many ant species, L. flavus feeds on the sugary 'honeydew' produced by aphids that are tended by the colony. However, the ant-aphid relationship is more complex than this as L. flavus has 'collected' a number of subterranean aphid species (e.g. of the genera Forda, Geoica, Aphis, Tetraneura and Baizongia) which, in Britain, have lost their sexual generation associated with woody plants and are now entirely asexual on the roots and stolons of grasses. Others such as Sappaphis bonomii lay over-wintering eggs on plants above ground, and L. flavus tends them as if they were ant eggs (at the wrong time of year). Not only that, but as well as using aphids as sources of honeydew, L. flavus also uses them as prey to feed its larvae (Donisthorpe 1927, Pontin 2005). The aphids rarely disperse openly above ground level, suggesting that despite the possibility of being eaten by ant larvae, the protection of subterranean ants outweighs this risk. Further, this may effectively form a type of 'culling', keeping aphid density below levels where they tend to start producing winged forms for dispersal.

So, although this is a common and widespread species, it hides a symbiotic lifestyle that is rarely seen despite taking place beneath our feet as we walk across many an old pasture or other undisturbed grassland. I'm certainly tempted to ask permission to investigate these churchyard mounds more closely and maybe learn more about the aphids and other 'guest' invertebrates that can be found within. As the church (St. Mary's, Bishopstoke) was consecrated in 1891, there has been plenty of time for the ant community to develop. Lastly, I want to look briefly at the landscape, or 'antscape', effects of L. flavus. In an old pasture, the anthills are close together (active ones may abut or overlap old inactive ones), but their arrangement is effectively patchy and random. In the churchyard, the association with graves means that this is not the case and the anthills are arranged more or less in a grid matching the positions of graves - even where these have since disappeared - in such cases the pattern of anthills marks the outlines of old graves - ghosts in the graveyard!

Pattern of L. flavus anthills following the locations of current and missing graves.

References

Donisthorpe, H.St.J.K. (1927). Guests of British Ants. Routledge, London. [An old classic; can be a bit expensive, and a lot of the taxonomy has changed, but still worth having].
Pontin, J. (2005). Ants of Surrey. Surrey Wildlife Trust, Woking. [Maps of ant distribution in Surrey, but plenty of other more widely applicable information about British ants].
Skinner, G.J. & Allen, G.W. (1996). Ants. Richmond, Slough. [An excellent little book in the Naturalists' Handbooks series. Includes species-level keys to the British ant fauna. If you want just one book on British ants, I recommend this].

Further reading

Agosti, D., Majer, J.D., Alonso, L.E. & Schultz, T.R. (2000). Ants. Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian, Washington DC. [Takes a global approach with particular emphasis on the tropics and Americas, but covers a range of widely applicable techniques and ideas].

Wheels of life

Straight in with a question today - have wheels evolved in nature? Now, I know it's been written about before, and there's no shortage of discussions on any number of online forums (or fora if you prefer), but it's something I've been musing on and coming up with some underlying questions - so, here goes with one my rare forays into the more speculative realms of biology and ecology...

Firstly, why might wheels be a useful adaptation? Well, they could provide an efficiency and simplicity of motion in some circumstances - I can certainly imagine animals using wide wheels to trundle across the soft sediments of the ocean floor for example (much like the wire-wheeled lunar rovers from Apollos 15-17). However, legs and fins generally work pretty well, with wheels really coming into their own on straight, smooth, hard surfaces. These are not common in nature, though humans produce plenty of them - and hence plenty of wheels. So, a lack of evolutionary advantage might be one reason why natural wheels are not widely seen.

Secondly, what do I even mean by a wheel? Here, I am only considering something that has an axle or bearing. There are plenty of organisms that roll - the South American pebble toad Oreophrynella nigra that tumbles down slopes to avoid predation, the wide variety of tumbleweed plants (and the rarer 'tumblefruits' such as Physaria) that disperse seeds as they roll with the wind, and the puffballs of the genus Bovista that are also blown around and so disperse their spores more widely. Ocean currents roll the coral Porites lutea across the sea floor and the small stomatopod mantis shrimp Nannosquilla decemspinosa can curl up and roll slowly like a wheel if stranded on a shallow damp sandy shore, thus returning to the sea. These are all interesting in their own right, and there are other examples, but none of them are wheels.

In fact, there don't appear to be any organisms that roll along on wheels in the way that humans' various vehicles do. As mentioned above, there may simply be no evolutionary pressure to produce a wheel, but there are also developmental constraints. For example, to have a wheel in a multicellular organism is tricky because, to be able to rotate freely, the wheel needs to be detached from the rest of the organism. If this is the case, how could it maintain a blood supply, neural connections and so on? Two options come to mind:

1. The wheel could be made of 'dead' material secreted by the organism, such as carapace material. This could grow as a toroid (doughnut-shaped) swelling on a limb/axle and gradually separate by thinning near the limb. This could produce a passive wheel on an axle much like a wood-turner produces a freely movable (but not removable) ring from a single piece of wood.
2. The wheel could be alive but self-contained. If a ring of cells developed as above and then detached, to be an effectively autonomous wheel, it would have to have its own energy supply (photosynthesis, chemosynthesis?) and so on.

Neither of these options have been discovered in nature, though this does not mean they never will - my feeling is that the lack of need is more likely to prevent wheels evolving than developmental problems. So far, I have not differentiated between passive and active wheels i.e. whether they simply roll like a cart (reducing the friction that would be caused by dragging) or are actively rotated by an energy source. Active wheels are developmentally even more problematic as a torque needs to be applied - in animals, motive force is produced by muscles, but this would not work on wheels as they need to be freely rotating. However, in bacteria, the problems of producing motive force, overcoming inertia and so on have been solved. In fact, the only example discovered so far of a true biological wheel (an active one that produces continuous propulsive torque around a fixed structure), is the bacterial flagellum, the  a propeller-like thread used for locomotion. Where the flagellum enters the cell membrane, there is a motor protein that works like a rotary engine, powered the flow of hydrogen ions (i.e. protons) across the bacterial cell membrane down a concentration gradient created by a proton pump. A similar system using a sodium ion pump exists in the genus Vibrio.

The structure of the flagellar base showing cutaway details of the 'motor'. Thanks go to Mariana Ruiz Villarreal for putting this and other diagrams in the public domain.

At an even smaller scale, the enzyme ATP synthase (which is involved in energy storage and transfer within cells) is somewhat similar to bacterial flagellar motors and is likely to be an example of modular evolution i.e. where two separate structures or sub-units (which evolved and previously functioned separately) become joined or associated, and in doing so gain a new function.

So, although true wheels have not been discovered in multicellular organisms, and both developmental and utility constraints make their evolution highly unlikely, maybe impossible, there are ways that wheels might be used in nature:

1. Through symbiosis, joining two otherwise unrelated structures/organisms in order to get round the developmental problems preventing direct evolution of wheels. This could be instinctive (imagine an extension of dung-ball rolling by dung-beetles) and is an idea which has been explored in fiction, e.g. in the Amber Spyglass (Philip Pullman, 2000). In this book, an alien race known as the Mulefa use large, round seed pods as wheels. They put these on sideways-oriented claws (which act as axles) on two of their legs, using the other two legs to push themselves along. The symbiotic aspect occurs because the trees that produce the seed pods depend on the rolling action under the weight of the Mulefa to break open the pods and allow the seeds to disperse and germinate. A number of other science fiction novels consider biological wheel use in a variety of ways, but Pullman's is probably my favourite so far, though other examples include David Brin's Brightness Reef (1995) and Infinity's Shore (1996), and Wheelers (2000), co-authored by Ian Stewart and Jack Cohen (who happen to be a couple of Terry Pratchett's collaborators if you like a bit of nerd-trivia).
2. Through tool use. Humans do this, using wheels widely - could other species do the same, even if with less technological sophistication? I'm just waiting to see corvids start rolling past...

OK, I think that's enough speculation for one day - if anyone out there does know of other examples of 'bio-wheels', I love to hear about them, so feel free to add a comment.