Call of Nature: The Secret Life of Dung

IN NATURE, NOTHING is wasted – not even waste. The throughput from herbivores is remarkably undigested, despite the range of complex digestive enzymes, acids and alkalis, convoluted and copious intestinal tracts, and the employment of countless millions of micro-organisms to break down the tough cellulose and complex plant chemicals. It’s all that roughage they eat. Typically only 10–30% of nourishment is taken from food into the average herbivore animal’s body; the remains are shunted out as dung. Sometimes nutrient absorption is as low as 5% – they’ve hardly touched their food. Omnivores, if they are following modern nutritional advice, also pass much that is still available for onward use by others.

Within the dung certain items, coffee beans for instance, or the sweetcorn niblets of schoolboy humour, pass through apparently unchanged. Baboons and birds frequently forage through elephant dung to get at any seeds that, protected by tough outer shells, have survived the digestive process. Throughout the world this type of behaviour is common, if only infrequently commented upon, with birds (sparrow, yellowhammer, chaffinch and linnet for example: Popp 1988) taking seeds and undigested oats from horse droppings, harvester ants removing fruit seeds from capuchin monkey faeces (Pizo et al. 2005), and spiny pocket mice taking seeds from cow and horse dung (Janzen 1986). Some seeds will only germinate if they have been passed through the gastrointestinal tubes of a large herbivore, or granivore bird (or both maybe). If the seeds escape these secondary feeders, they benefit by being scattered away from the potentially overshadowing parent bush, and the seedlings will end up further separated, diluting any obvious competition with each other, and enhancing future genetic diversity. The further seed dispersal abilities of dung beetles will be looked at later.

Seeds aside, most of the content of elephant dung is little more than semi-processed leaf material, cut into convenient short pieces, partly chewed to a soft consistency and certainly only partly digested. A small group of four or five elephants can take a tonne a day of rather inaccessible coarse herbage, tear it down, mash it up and deliver it in neatly arranged parcels at ground level, where it is now available for many others to use. In Central Africa, the sitatunga or marshbuck, a type of deer, forages on living shoots and leaves, but also gets a significant part of its nutrition, seeds and chewed herbage, from elephant dung, appearing out of the jungle as soon as the fresh droppings are released. It’s getting as much from these deposits as would a cow from the farmer’s morning presentation of hay or silage.

Fig. 13 The marshbuck, or sitatunga, considers elephant dung as just a convenient silage drop.

Elephant droppings provide a good baseline model for understanding the immense biological importance of dung. That it is important is in no doubt, since huge numbers of dung beetles (and flies) swarm in to any available dropping. Incidentally, in the identification gallery (chapter 12) later on, it is obvious that dung-inhabiting insects come in many shapes and sizes, but for most purposes ‘dung beetle’ refers to any of the approximately 9,000–10,000 species of short, squat, rounded or cylindrical, powerfully built beetles in the hugely diverse families Scarabaeidae, Geotrupidae and Aphodiidae. It is these beetles which will get the lion’s share of attention throughout the rest of this book. I admit that this is partly because I find dung beetles fascinating; they are handsome and charismatic. But also because a natural history of dung can readily be distilled down to a natural history of dung beetles. I will, however, try not to let this bias take over too much. Anyway, back to elephant excreta.

There are verified reports of nearly 4,000 dung beetles arriving at a half-litre sample exposed for 15 minutes – that’s nearly four and a half beetles per second (Heinrich and Bartholomew 1979b). In a timed study, a 30 litre pile (think large kitchen bin) of elephant dung was reduced, in under half an hour, to a spreading fluidised layer of squirming beetles, covered by a thin rind of fibrous material, the insects reducing the beachball-sized heaps to a nearly circular mat 2 metres across and 2–3 cm deep. Elsewhere 16,000 dung beetles spirited away 1.5 kg of elephant dung in under 2 hours (Anderson and Coe 1974). The literature of dung beetles is littered with these astonishing figures. Dung beetles are keen, very keen indeed.

Such observations are not limited to the tropical savannah. In a pitfall trapping exercise in Langley Wood, Wiltshire, Michael Darby was more than a little amazed to find his sampling pots jam-packed with one of the dor beetles, Anoplotrupes (Geotrupes) stercorosus, every time he emptied them. The dors are northern Europe’s largest dung beetles and although widespread you seldom find more than one or two under a cow pat or horse dropping. He was finding hundreds at a time in the small pitfalls, and between August 2006 and July 2007 had counted over 20,000 specimens (Darby, 2014).

I can’t quite compete with that, but on the South Downs of Sussex one hot August day back in 1974 I watched a cow pat, just a day or so old, heave as several hundred small mottled dung beetles, Aphodius contaminatus, jostled together in the congealing semi-fluid interior under a thin rind of dried dung.

Typically one elephantine bowel evacuation lands in a large heap weighing 10–20 kg. This is a finite amount, and although a massive volume compared to even the largest dung beetles (weighing about 20 g), these insects must act quickly if they want to use it. Latecomers will find that they are just too late. The important ecological imperative here is not that they are going to eat much of it (in fact adult dung beetles eat very little, see page 70), but that they need to secure a large enough portion of it to see any of their offspring through from egg to adulthood.

However, if the beetles simply arrived, mated and laid their eggs willy-nilly, it is quite likely that within a very short time the resulting larvae will have devoured all the available dung, even a massive elephant deposit, long before they are mature enough to pupate and metamorphose into adults. They would all perish. This would not be a very successful evolutionary strategy. Dung-feeders have evolved various means to carve up the dung pie, as it were, and these will be looked at in more detail in the next chapter. What is important is that they actually do get a part of the pie, and that they get it quickly.

I recently had a welcome occasion to study British dung beetle eagerness first-hand. The beetles were arriving at a freshly dropped stool (that would be stercore humano in ultra-polite parlance) one warm May afternoon in 2015. The site, a former railway sidings and shunting yard, had been partly developed and landscaped with mounds of soil, gravel, crushed brick and concrete, to create an ‘ecological area’ for native wildlife; it had greened up a bit since the municipal recycling centre had been built, with a thin haze of scant herbage, but was well away from any grazing animals, meadows or indeed green fields in any conventional sense. It was here, in a private corner, that I was able to conduct an experiment in the island biogeography that best exemplifies just how incoming colonisers find a tiny portion of suitable habitat in a sea of barren wilderness. In less than 30 seconds from deposition the first dung beetle had flown in and was hovering over the deposit. At just under 3 mm, Aphodius pusillus is one of Britain’s smallest dung beetles, and was probably more used to the rabbit pellets amongst the sparse vegetation of the site. But it was not alone.

Within 15 minutes, over 50 beetles, comprising nine different species¹ had arrived by air, along with a loudly buzzing selection of blow flies. This partly begs the question where all these coprophagous insects came from to arrive so quickly at a large omnivore dropping where previously there had been no obvious community of dung-producing animals to supply their needs. None of the beetles was particularly large, but several were in the 6–8 mm range, suggesting that rather than rabbit crottels it was horse and cow dung that had sustained the thriving populations hereabouts, and that they had probably travelled many hundreds of metres since leaving the farmland where they grew up. It seems highly unlikely that they had all been busy at work in a meadow half a kilometre away to the south, when they suddenly caught a whiff of something tasty in the air and decided to investigate; these were beetles already somewhere in the close vicinity, they had been active, on the wing, possibly even cruising on the lookout for new supplies. They had been rewarded, and an hour later the dung was riddled with an eager mass of beetles.

Others have carried out similar experiments, albeit accidentally. When coleopterist Clive Washington had to call in a drain company to unblock his household sewer, removing the manhole cover revealed a logjam mass of putrid brown sewage. Within 10 seconds Aphodius were flying down and landing beside it, much to his delight.

On holiday in Costa Rica a few years ago, I took whatever opportunity I could to examine the droppings I came across in the tropical rainforests (I didn’t add any of my own on that occasion). There weren’t that many – a few meagre nuggets from deer, monkeys and peccaries. Many had a selection of dung beetles hollowing them out from the underside. These were mostly small, squat, smooth, round, slightly metallic scarabaeids. I also found the same beetles sitting on leaves in the shafts of dappled light reaching down from the canopy to the forest floor below, where they seemed to be perching, antennae outstretched all aquiver – waiting. Canthon viridis is well known for being very keen, and this perching behaviour is frequently reported. It is, figuratively at least, on its marks ready, set to go, as soon as it detects the chemical scents from a dropping being freshly dropped.

Fig. 14 The splayed antennal club is a sure giveaway that the beetle is detecting faecal scents in the air.

That dung beetles smell out the dung has long been known. When they arrive at a fresh pat, they invariably fly upwind, following the trail of scent that the breeze is bringing down to them. This is an observation which can be repeated by any keen scatologist reader in grazing meadows all over the world. Larger beetles can be seen zigzagging in to the target; they are programmed to fly forwards if they can smell their quarry, but move left or right if they lose the scent for a moment, until they find themselves back in the airborne plume. To visualise this process imagine that you’re seeking a smoky bonfire, but that you are blindfolded. If you can smell the smoke you move up into the wind that brought the soot into your nose. But if you step outside of the irregular wafting smoke stream, your best bet of finding it again is to move increasingly right and left, scanning the scentscape perpendicular to your previous route, until you step back into the cloud. Then you set off windward again. This is exactly what scenting insects do when flying towards their quarry.

Dung beetles don’t have noses; their antennae are olfactory organs. The last few segments (usually 3–5 of them) of the antennae are flattened and expanded into a series of plate-like slices (lamellae) forming a broad club. This greatly increases their surface area, and thus also the number of submicroscopic chemosensitive receptor cells which cover them. These highly sensitive pit- or hair-like structures allow the beetles to smell airborne molecules at incredibly low concentrations – we’re talking parts per billion here. Males and females have similarly shaped antennae, suggesting that it is food they are smelling out. In other insects large, highly sensitive, feathery antennae are usually associated with only one gender, which needs the extra smelling capacity, afforded by increased surface area, to detect sex scent pheromones released by prospective mates. Some dung beetles do use pheromones to communicate between the sexes, but finding each other happens at the dung source, so their most important olfactory test is to find the dung in the first place.

Recent electroantennographic research, using isolated antennae in micro-windtunnels, has allowed direct electrical measurement of nerve impulses as different test chemicals are wafted past. Dung beetle scent receptors responded to a range of dung volatiles, including our foetid friend skatole, and other similar bacterial decay molecules such as 2-butanone, phenol, p-cresol and indole. Butanone seems to be one of the most important of these molecules; it’s certainly the most volatile (boiling point 79.64°C) and has the simplest molecule CH₃C(O)CH₂CH₃ (methyl-ethyl-ketone), whereas the others have more complex ring structures. According to some researchers, isolated and concentrated butanone smells of butterscotch and nail varnish remover (Tribe and Burger 2011).

It seems likely that dung beetles are not simply attracted to just one chemical, but their antennae are sensitive to the melange of different odorants given off by decay. This is useful because it means that dung beetles can be attracted for sampling purposes by the simple expedient of plopping some excrement on the ground. But the fact that each type of chemoreceptor on their antennae reacts to just one type of airborne molecule does, however, throw up some unusual observations. Michael Darby’s 20,000 dor beetles were not attracted to dung; his traps were unbaited, but were laced with a small amount of ethylene glycol. This is standard car antifreeze, and as well as being cheap and easily obtained, it makes a convenient preservative in pitfall traps. What may have been happening is that the dor beetles were attracted to the corpses of other insects fallen into the traps (ground beetles especially), which were releasing similar, but non-dung organic decay molecules. Who knows, maybe 2-butanone was among them. This created more corpses, which escalated the effect, leading to the huge numbers of dors eventually accumulated. Elsewhere among dung beetles there are strange examples of species being attracted to chemicals that are not given off by dung, and this has led to dung beetle evolution away from dung to use other food sources. More on non-dung beetles later.

Though they smell the dung from way off, dung beetles use eyesight to target the dropping when they get close. There is a neat relationship between small beetles (with small eyes) which fly by day and can land accurately in daylight, but large beetles (with correspondingly bigger eyes) having the greater optical capability necessary to fly at night. Day fliers are fast and sure, but night flights offer the problem of hazy obstacles, difficult to make out in the gloaming. Slow fliers might open themselves up to predators such as owls and bats, and sure enough nocturnal dung beetles tend to fly fast but sloppy.

Dung beetle eyes are protected by a bar across the middle, on a line with the broad shovel-like plate that defines the front of the head. Called the canthus, it sometimes nearly divides the eye into two, and is thought to offer some defence against abrasion to the eye when digging through the soil, a bit like bull-bars on off-road vehicles might protect the headlights against knocks. Nocturnal species, needing all the visual help they can get, have the canthus smaller, or absent, so more eye is available to catch the fading rays.

These observations of manic arrival at the pat typify the struggles which all dung-feeding insects face – that dung is a rich organic food, but it is produced sporadically, in a random, widely spaced scatter across (to an insect) a truly vast landscape, and that the small dropping from anything other than an elephant is barely enough for a few individuals to raise just one generation of offspring. In ecological jargon, dung pats are regarded as patchy and ephemeral microhabitats. In order to find them before they have decayed, or dried out, dung-seekers need to be active, adventurous and willing to take to dangerous skies full of wayward winds and hungry predators, expending energy and possibly risking their lives, if they are to find a competitor-free food source for the next generation.

It’s slightly cheating, but some dung beetles don’t need to find the dung themselves, they are brought to it by the dung depositors. It is immensely sad that the common name ‘sloth anus beetles’ has not been universally adopted for the genera Uroxys and Pedaridium (formerly Trichillum) which, as their name might suggest, hang around on hairs near sloth anuses, waiting until sloth defecation takes place (Ratcliffe 1980; Young, 1981b). Similar beetles in the genera Glaphyrocanthon, Canthidium and Canthon loiter near monkey anuses, and several Onthophagus species cling to the nether orifices of wallabies and kangaroos. They have specially adapted prehensile claws to stick tight.²

Fig. 15 It took entomologists some time to work out how the tiny (3 mm) Pedaridium sloth beetles lived. They travel in the coarse sloth fur, but hop off to lay eggs each time the host descends from the trees to deposit some dung on the ground.

However they arrive, dung beetles will have to compete against similar-minded contenders for the resource. Even if they succeed in getting there and laying eggs, their offspring will have to struggle against the demands of all the other dung inhabitants, including each other. Too many of them, and they will, quite literally, eat themselves out of house and home. They need to find the dung and get in quickly, they need to stake a claim, and at the same time they need to ensure that they will not overburden the very limited food resource they have been offered.

It turns out that although dung beetles are highly mobile (apart from the anal hangers-on), energetically active and quick to home-in on fresh faeces, they are not overproductive in the egg department, and that they do not, as it were, breed like flies. Actually, flies also have similar pressing needs when it comes to securing a dung-sufficient future for their maggots. We’ll come back to flies a bit later.

Of the few species that have been studied closely, an individual female dung beetle is highly unlikely to lay more than a few dozen eggs during her lifetime of many months. And although some of the smaller general dung-feeders may eventually manage 150 eggs, many of the large exotic dung-rollers that rush in to an elephant dropping are only ever likely to produce 5–20 offspring each, often only one at a time. The nesting behaviour, examined more closely in the next chapter, where individual buried balls of dung are attended by a guardian female, appears to have an egg-suppressing physiological effect on the beetle herself, delaying any further eggs in her ovaries from becoming mature until she is convinced that she has done all she can there and is ready to move on to start again. Already there are self-limiting restraint mechanisms at work here, to prevent single dung pats being overwhelmed, to the detriment of all.

A self-evident indication that dung is a valuable natural resource is the fact that dung-feeders not only swarm up to it as soon as it lands on the ground, but that they are apt to fight over it when they get there. The petty squabblings of dung flies will be looked at again shortly, but some dung beetles have armed themselves with quite formidable weapons in the long evolutionary battle for niche supremacy.

The ridges, humps, bumps, spikes, spines, horns, prongs and antlers borne by many male dung beetles are some of the most extravagant body decorations in the insect kingdom. They range from the stout but elegant single head horn, through bulbous spikes and ridged skewers, to flanged and fluted art nouveau protuberances, and they’re well worth looking at if you need inspiration for an unusually gothic Hallowe’en costume. The fact that it is generally males that carry these weapons, and that they are attached at the front end – head and thorax – clearly supports the idea that they are used in fights. They’re analogous to the impressive antlers sported by male deer, though unlike testosterone-pumped bucks during the noisy and dangerous rut, dung beetle head-to-head attacks are rarely witnessed.

There were some suggestions that these over-exuberant horns are the result of sexual selection – choosy females choosing only to mate with the best endowed males. Charles Darwin first mooted this idea in 1871, imagining that these horns became ornately developed through natural selection in the same way that increasingly bigger and brighter peacock tail feathers were chosen by an ongoing selection of particularly picky peahens down the millions of generations. However, morphological and behavioural studies now suggest that dung beetles’ wondrous projections are genuinely used for combat. These are jousting and wrestling contests, pushing and straining, rather than the insect equivalent of sword fights, and the contests take place between males of the same species.

It’s worthwhile spending a little time examining dung beetle horns, because they are truly fascinating. They’re beautiful, weird and there are some very interesting ecological lessons to be learnt from their study.

Different dung beetle species will have different approaches to using the dung, different techniques in extracting it, different needs in terms of size, density and moisture content of the dung. They may compete, one species against another, but such scores are usually settled by subtle ecological and behavioural differences – they arrive at different times of day, or in different seasons, they may live in different places, or take different portions of the pat. On the other hand, beetles of the same species will have directly competing needs, and it is this within-species conflict that has given rise to the dung beetle tusk-based arms race. Simmons and Ridsdill-Smith (2011b) and Knell (2011) give good overviews of horn evolution and development.

The very large genus Onthophagus, with upwards of 2,500 species worldwide, provides plenty of good examples, with something like 10 different standard shapes of horn or antler, arising from 25 different zones of the anterior body surface of the beetle. These different sizes, and combinations of head and thorax horn, create an almost infinite number of permutations, much to the delight or consternation of the taxonomists trying to identify these beetles. Many a time I’ve pored over the microscope, trying to convince myself, or not, that the subtly different spike shapes on a series of Onthophagus coenobita males represented different species, or different subspecies even. Frustration and delight in almost equal measures. Numerous dung beetle researchers brazenly assert that Onthophagus is the most species-rich genus anywhere in the animal kingdom. There certainly are a lot of them, but rival claims are also made by jewel beetle (Buprestidae) specialists for Agrilus, arguing 3,000 species. I’m not going to take sides in this discussion, but I suspect arguments over the validity of genera, subgenera and species groups could keep these two clans at loggerheads for some time.

And keeping each other at loggerheads (see what I did there) is just what the beetles do when they fight over the dung. Actually, they fight under the dung. Whatever their weaponry, two dung beetles meeting face to face on a flat laboratory surface fail to engage each other, but in the confines of a burrow, or space under the dung, head-to-head conflicts can now escalate. The beetles can shuffle, one left, one right, or one upside-down compared to the other, and the horns and ridges now make full contact with each other. They can lock against one another, just like the spike-and-bar projections of a handheld bottle-opener prising off the cap from a recalcitrant beverage. These contests of strength can last 75 minutes.

Fig. 16 Engraved plate of Onthophagus species from the famous Biologia Centrali-Americana (Bates 1886–1890).

In the tunnel, push comes to shove now, and leverage applied by the head and thoracic horns becomes paramount, as well as their exact shape and length. In the squat, stout, muscular frame of a dung beetle, leverage is a function of body size, and body size is a direct consequence of nutritional intake during the beetle’s larval stage. Within any population of a given dung beetle species, body size can vary by a factor of two or more, with smaller individuals barely half the size of their relatively gigantic confederates, even within the same pat, and in the same group of siblings. This size differential is reflected in the relative sizes of the horns too. Along this spectrum of body sizes of a given species, from small to massive, horns also vary from non-existent to monstrous. And it’s mostly down to food intake as a grub – how much they got of that all too precious commodity in the dung pat.

The exact amount of nutrition received as a larva depends on dung quality as well as quantity. It also depends on temperature; feeding, digestion, metabolism and development proceed faster in warmer seasons or warmer climates. Thus, there is no fixed formula that states a larva must feed on so-and-so amount of food, for such-and-such a time, then change into an adult. But, even in the face of a low-quality diet, a limited amount of food, poor weather or northerly location, a larva can’t just go on morosely eating and eating until it has finally had its fill. It may miss a vital synchronisation window with potential mates, it may emerge too late in the season to find suitable new dung, and the longer it goes on being a soft vulnerable larva, the more it exposes itself to the dangers of predators, parasites and disease. There is a pressure to get on and become adult, no matter how large or small you may be as a larva. At some point the decision to become an adult beetle, no matter your size, has to be taken.

Surprisingly there is not a direct proportional relationship between full adult body size (i.e. larval food intake) and overall horn length. Certainly the largest males of a particular species have the longest horns, but in the middle of the body size range in this species, the horns of apparently similar-sized beetles can vary from nearly maximal to almost non-existent.

This plasticity is a result of how the horns are produced in the metamorphosing pupa. Unlike, say, a leg, which is clearly defined in terms of size and shape and proportions by fairly strict genetic control, the horn is highly variable. It starts as a simple flap of cuticular skin as the beetle’s adult shape takes form inside the chrysalis. Clusters of cells detach and proliferate, folding as they become trapped under the larval skin, but then expanding as the final moult gives way to the pupa. The embryonic horn sometimes looks like a series of concentric wrinkles, telescoped inside each other. But the final decision to go ahead with a prominent spike can be deferred until the last minute, or even reversed. As metamorphosis progresses, the horns can be remodelled, in both size and shape. In some species, programmed cell death, under hormonal control, can completely remove a horn apparent early on in the pre-pupa (especially one on the thorax), so that the adult beetle emerges surprisingly hornless. This also gives rise to the occasional horned sport, where no horn was known before.

The appearance, or not, of a prominent horn is not completely random. There appears to be a cut-off threshold at which point, after feeding has ceased, the beetle metamorphosing inside the pupa suddenly feels it can invest, after all, in a nice show-off spike. This threshold is under some genetic influence, and isolated genetic populations show slightly different patterns; thus in North Carolina most specimens of Onthophagus taurus (two bull-like head horns, obviously) over 5 mm wide have horns 4 mm long, whilst in Australian colonies they have to reach about 5.25 mm across the thorax before they can achieve such horn prowess (Moczec 2006).

Perhaps more surprisingly, a mid-sized dung beetle larva, changing into a mid-sized pupa, which might be expected to display a mid-sized horn, may actually emerge as a completely hornless male. This decision may be made right at the last minute, with potentially horn-enabled cells being reabsorbed and redestined, rather than being predestined from the outset. It seems there is some benefit from not showing off what would likely only be a modest tool after all, but in reallocating the horn material during metamorphosis to become a slightly bigger, if weaponless, rather effeminate, male.

These ‘minor’ males (as opposed to the brawny ‘majors’ with their swaggering body embellishments) nevertheless can get a piece of the dung action. They do not need to engage in loggerhead scuffles with other males. With their demure female-like hornless disguises, they can waltz right past, seemingly unobserved, and sneak-mate with the real females whilst the tusked warriors are otherwise engaged, battling it out with each other or shearing up the burrow walls and shaping the dung brood masses. Nutrition is all, but there are ways round any horn loss occasioned by not quite eating enough of the pie. The physically emasculated minor males can still gain sexual access, to pass on the genes that control, if necessary, horn reabsorption in the interests of false humility.

The clincher, if clinch were needed, occurs in two African species: Heteronitis castelnaui and H. tridens. These are the only known dung beetles where it is the females, rather than the males, which have the larger horns. In these species it is only the females that dig and burrow, and only they that remain in the tunnel to guard the brood balls of dung. Consequently, it is not the males that might need to fight over females, but females that fight over buried dung resources.

Fighting horns do appear in other groups. The aptly named minotaur beetle, Typhaeus typhoeus, is a dumbledor (family Geotrupidae), but is armed with three prominent thoracic horns in the males (small bumps in the female). Like Onthophagus appendages, they can vary from menacing spear-like prominences to rather feminine protruberances, and the assumption must be that they also fight, or sneak, in the deep tunnels they burrow. In Africa, where everything is bigger and more ferocious, males of Aphodius renaudi, are the only known examples of horn-bearing in this usually demure dweller genus of dung beetles.

Dung-rolling beetles will also fight with each other, but these are generally tussles over a dung ball, and here body size and leg length is everything. There is wrestling and pushing, flipping of heads and flailing of limbs, but without the constraining walls of the tunnel to allow locking of antlers, there is no tight head-to-head locking of weapons. Consequently roller males do not have horns. There’s no point.

It’s not always easy having horns. The many bizarre horn shapes, their variation between individuals of the same species, and the useful identification features they provide to distinguish between species have led entomologists to invest much time in studying dung beetle appendages. For one thing, not all groups have them; as discussed earlier, they are most prominent in the genera that burrow in the soil under the dung, rather than those which merely wallow in faeces, or roll away balls of the stuff. They have evolved at least eight times in tunnelling dung beetles, but for each group with horns there are others, some closely related, lacking them. Having horns is not, in itself, a necessity for evolutionary success. Like many animal fight contests, real damage to each other is often avoided because one of the contenders very soon realises it will fail and gives up before blood (or haemolymph) is spilled. This usually takes only a few minutes. The other then celebrates victory by keeping or taking possession of the buried dung ball, the female, or both. But even though no body-wrenching clash of weaponry actually takes place, this doesn’t mean that the horns become trivial – they are no mere costume pretence, they are very real and building them takes a real toll on the beetle’s physiology. In fact, there is a significant biological cost to having horns (Harvey and Godfrey 2001).

Fig. 17 Onthophagus taurus plate, from the seminal British Entomology (1823–1840) by John Curtis. The flower was merely an artistic juxtaposition – possibly more aesthetically pleasing for subscribers to the work than a cow pat.

Careful measurement of horn lengths within a species, and comparison with other body features shows that larger male head horns are associated with relatively smaller eyes and/or antennae (20–28% loss reported), as the limited resources within the developing pupa are traded off against each other (feeding has finished after all). Likewise, hornless females have relatively larger eyes than their horned consorts. Similarly, as thoracic horns increase in size, they are met with a comparative diminution in the beetles’ wings (Moczec and Nijhout 2004). Here is a dangerous gamble (with life-changing consequences) made at the pupal stage, before the adult beetle has emerged. Anyone who has ever played computer games will recognise this choice when deciding on a character at the beginning of a contest – at its most basic this can be a choice between smaller and faster, or larger and more powerful. The dung beetle has to make this character decision without knowing what the world out there holds for it. The long-horned beetle major is hoping, perhaps, that pats will abound, that it will not have to fly too far on its slightly smaller wings, that its slightly reduced visual acumen and sense of smell will still allow it to find a suitable dropping. The rewards for the gamble succeeding are that when it arrives at the pat it will have a better chance of jousting its competitors out of the way, securing the brood ball and the female, and that the dung will be, as it were, its oyster. On the other hand, if the dung pats are sparser, a svelte hornless minor is, perhaps more able to complete its challenging quest on bigger, stronger wings, using its sharper eyesight and keener sense of smell to arrive at a distant dropping ahead of its clumsier, more obtuse fellows.

Perhaps the most remarkable trade-off is between opposing parts of the beetle’s anatomy. It seems that increased horn size is directly correlated with decreased testes size. So those show-off bullies – you know, the ones with the biggest weapons – they really are compensating for something (Simmons and Emlen 2006). The evolutionary logic goes something like this. A well-endowed beetle can afford smaller testes because the beetle will easily achieve a suitable mate, and its sperm, though meagre, will be well targeted. After mating it will be capable of guarding the female so no further matings will dilute his sperm that she is storing. His small investment will be protected, and successful offspring will result. On the other hand, lesser-horned males may have to make do only with sneak matings, they must squander their seed, so their best evolutionary chance of success will be if they can use their copious sperm to mate with multiple females to try and sire at least a few offspring through sperm dilution.

It is not just with each other that dung beetles have to fight (literally and figuratively). They also have to battle the weather, most notably the heat. Insects, even large stout beetles, can only burrow into the dung, mould it, shape it, manoeuvre it and feed on it, when it is moist. As soon as it starts to dry out, the mushy fibrous mix starts to clag into a hard impenetrable mass with the texture of concrete (hence its suitability for a human building material), or else it becomes brittle and friable, disintegrating into dust and loose fibres. And as it dries out, so too the tell-tale volatiles that attract the dung inhabitants dry up; dry dung is no longer attractive because it no longer has the chemical scents that attract. This, of course, is another reason why there is the mad scramble to arrive at the new pat. Freshness is all.

On the whole, the coarseness of the dung’s texture, and the precise fibrous make-up of the dung, a result of what the animal was eating before it voided, is of less consequence than the liquid and submicroscopic components in the moisture of the dropping. Obviously it is the adult insects that arrive at a fresh pat, and despite the fact that dung beetles have chewing mouthparts, they are not equipped for much crushing, grinding and chewing of fibre particles; they concentrate on sipping the delicate juices of the dung.

From a neat series of experiments using various precisely engineered glass or latex beads of differing sizes, it is clear that even the largest adult dung beetles ingest only the smallest particles (8–50 μm diameter); they partake of the dung soup course only (Holter and Scholtz 2007). This is, nevertheless, highly nutritious, containing fermenting matter already half-digested, free-floating organic compounds and nutrient-filled bacteria beyond number. They lap this up as soon as they arrive, and despite my slightly facetious culinary quip about soup, this is a necessary and fortifying meal for any newly emerged dung beetle female. In the rush to get through larvahood, then manage the metamorphic change during pupation, and emerge as a fully functioning sexually reproducing insect, the resulting female’s body size is just as influenced by the nutritional intake of the larva as the male’s. But whereas a male beetle’s horn size and shape is fixed and final, the female is able to extend the nourishment getting to her ovaries by continuing to take in food for herself. This maturation feed at the fresh dung is an important prerequisite before any thought of mating, nesting or egg-laying behaviour. After egg laying she will feed some more to mature a new batch of eggs ready for the next pat in a few days or weeks time. As the dung dries out, though, the soup becomes harder to find amidst the drying fibrous mass, and the dung beetles are unable to get enough nutrition. Eventually they give up and move on.

Flies do not have any jaws at all; their mouthparts are purely for sucking, so they too are only after the soup segment of the dung meal. It is not long before a pat, previously invisible under its bristling shroud of fussing and tumbling flies, is silent and bare. As soon as the outer layer dries and a crust forms the adult flies are unable to gain any more liquid nourishment. The occasional straggler may be able to find a crack in the crust, or explore just inside an entrance burrow of a beetle, but on the whole the dung is now left to the flies’ maggots to consume from within.

Contrary to popular expectations, damp dung also attracts butterflies. Like flies, these are drink-only insects as adults, and although the coiled tubular proboscis is more familiarly thrust down into a flower nectary, many species have been recorded feeding on horse droppings, cow pats and dog dung. They tend to visit on hot days when the fresh dung is at its most fragrant, and perhaps when they are most in need of liquid refreshment. I’ve seen chalkhill blues, small tortoiseshells and a comma feeding on fresh dog dung, and although I know what they’re after, it’s always a novelty to see these pretty fluttering insects so seemingly out of place. In Britain the purple emperor is more often seen feeding on dung than any other foodstuff, mainly because it does not visit flowers at all. Instead of nectar it subsists, as an adult, solely on liquids obtained from animal droppings, carrion, fermenting tree sap, rotten fruit and muddy puddles.

In the tropics dense clouds of butterflies, frequently many different species together, settle on the wet mud at the sides of streams and ponds where cattle or antelope drink, and which have been liberally splattered with the animals’ dung and urine. Such behaviour is called puddling, and the insects appear to be obtaining vital nutrients such as mineral salts, sodium and ammonium ions, amino acids and simple carbohydrates.

One of the most unusual instances of dung-feeding occurs in the Egyptian vulture, Neophron percnopterus, which occurs as various subspecies across southern Europe, Africa, Arabia to the Indian subcontinent. In Spain, the vulture is called churretero or moniguero, names which mean ‘dung-eater’, because of its conspicuous coprophagy. The normally meat-eating birds do not obtain protein (<5% in dung) or fat (<0.5%) from the cow, sheep and goat droppings, and the undigested cellulose would be alien to their digestive system anyway. They are after carotenoids. These are natural yellow pigments, mainly made by plants and bacteria, which the birds cannot biosynthesise themselves, and which they can only otherwise find in eggs or a few insects; these are unreliable sources where the vultures scavenge. Dung, however, is freely available, and contains the carotenoids the birds need (Negro et al. 2002). The pigments are important to the vultures, which have bright yellow beaks and faces, free of feathers, which indicate dominance status and are used in mating displays. Again, though slightly indirectly this time, you are what you eat.

Using dung as a food source is the major motivation for most animals’ scatological interest, and this will be the central theme for the rest of the book. However, before concentrating attention solely on coprophagy, there are a few minority dung uses which bear scrutiny. These are not accidental dung uses, just those that have not quite made it into the mainstream yet.

Dung makes good bait. Wasps of various species regularly haunt fresh droppings, but they are not after the moist faeces themselves, more the other insects also being attracted – upon which they prey. The digger wasp, Mellinus arvensis, will sit atop a new horse dropping and pounce on the many dung-flies that are attracted. There’s a video of one hunting around a badger latrine, available on the internet. Like all wasps, it’s a predator, stocking its nest with the remains of its dead insect victims for its grubs to feed on. The nest burrow (well away from the dung) may terminate in a half-dozen cells, each stocked with 4–13 flies. As with many predators, once one attack is successful, the wasp learns from its triumph and returns to the same site repeatedly, to collect food, and it will revisit the same dung constantly throughout the day.

I once watched social wasps (yellowjackets) Vespula germanica trying to hunt down dung beetles arriving at a fresh patch of ripe dog dung on Hampstead Heath (Jones 1984). There were several wasps, and they made many unsuccessful attempts to grab the small mottled beetles, Aphodius contaminatus, which were busily flying in. Although they met their intended victims in mid-air, the wasps were obviously not quick enough to get in a fatal bite, before each flying beetle folded up its wings, closed its tough carapace wing-cases, and dropped into the grass to continue its mission on foot. And yet with six or eight wasps in attendance, they must have been having some success, presumably with the greenbottles and blow flies that were also being attracted.

The hornet robber fly, Asilus crabroniformis, rarely misses though. This large handsome brown and yellow insect, one of Europe’s largest flies, is a fearsome adversary, and can bring down a flying dumbledor (Geotrupes species) with its massive spear-shaped mouthparts. Dung beetles make up a fair proportion of this robber fly’s prey items, since it has a penchant for launching its attacks from drying cow pats. I don’t think egg-laying has ever been observed in this species, but it is strongly associated with grazing meadows, where the predatory larvae live in the soil around cow dung, probably feeding on dung beetle grubs and dung-fly maggots.

Several types of beetle are also predators, but rather than using the dung as an attractant bait and waiting for prey to fly in towards it, they are more established as part of the in-dung community, so will be looked at in the next chapter.

The use of dung as a house-building material is, not surprisingly, also found in nature. The black lark, Melanocorphya yeltoniensis, and to some extent the sociable lapwing, Vanellus gregarius, have a strange habit of arranging a tumbled pavement of dried horse or cow dung pieces around their nests, on the grassy steppes of Kazahkstan and Russia (Fijen et al. 2015). This ‘decoration’ has produced quite some discussion amongst ornithologists. It seems to be something more than the birds merely using whatever available material they can find to create a suitable dish-shaped cavity on the ground to contain the eggs. They seek out the dung and use it in a defined way to create a closely laid patio around the nest. In the black lark, especially, the orientation and density of the dung pieces around the edge of the nest is predominantly coordinated in a north-east direction, suggesting that there may be some climatic or weather-related reason for the arrangements. One suggestion is that the dried dung pieces absorb the sun’s heat during the day, and buffer the cold north-easterly winds during the night. A sort of night storage heater for the birds. Elsewhere the incorporation of dung into bird nests is common, and well known in blackbirds, thrushes and robins, who frequently line the inner bowl of their twig and grass constructions with the dry, soft vegetable fibres.

A particularly niche building application occurs in the larvae of various leaf beetles, which use their own droppings to disguise themselves. Most remarkable among these are the tortoise beetles. The adults are gently domed and flanged around the edges, very tortoise-like. They are able to hide their legs and antennae, retreating under the hard carapace of their thorax and wingcases if attacked, but their strange spiny larvae use an umbrella of their own stringy faeces under which to hide. The palmetto tortoise beetle, Hemisphaerota cyanea, collects a lifetime thatch of extruded excrement over its back, and looks more like a disembowelled ball of string than a living creature (Eisner and Eisner 2000). Other species are less flamboyant with their faeces, but even the common European green tortoise beetle, Cassida viridis, manages to collect a knob of brown and black frass which it holds over its back on the aptly named faecal fork – a long, pronged, hinged structure at its tail end. The advantages of your own dung parasol are probably twofold for the beetle larva: the dark twiggy strands make the creature look wholly uninsectlike, foiling any bug-shaped search-image used by birds, which are mainly visual hunters, to find prey; the dry brittle stalks are also unpalatable to these birds, which were no doubt hoping for a plump moist morsel, rather than an animated brillo pad.

Slightly less precisely engineered, but nevertheless equally effective, lily beetle larvae manage to completely cover themselves with their copious semi-liquid droppings, by virtue of having their anus halfway along their back. The shiny red-brown slug-like larvae become almost invisible in the rough jumble of slimy red-brown faeces that coat the leaves as these notorious garden pests shred the gardener’s prize blooms. In the UK this is the black-legged Lilioceris lilii, but in much of Europe there is also the red-legged L. merdigera, from the Latin merda and geros meaning ‘dung-carrying’. The excremental coating serves to hide the larvae from bird predators. Parasitoid wasps and insect predators are also deterred by the gluey mess, which gums up their legs, antennae and jaws should any of them be foolish enough to get too close. And I wouldn’t be surprised if pesticide sprays are also deflected by the layer of dung insulation.

Several genera of leaf beetle in the subfamily Cryptocephalinae are called pot beetles, because the larvae live inside a hard or leathery pot made from their own frass, with just their front legs and head poking out at the front. As each egg is laid, the female beetle, dangling from a leaf, coats it with a layer of faeces (a process called scatoshelling), patting it down hard and even with her back legs before dropping it to the ground. The larva eats fallen leaves from the foodplant, adding to the rim of the pot as it grows, and only abandoning it when the new adult beetle emerges from its pupa. The pot cleverly hides the vulnerable grub, which just looks like a small particle of soil amongst the real soil particles. An even more advanced bit of coprocoating occurs in the closely related Clytrinae leaf beetles. Here the dropped frass-encrusted eggs are picked up by ants, confused by chemical signals from the larva, and taken back the nest, where the pot-laden grubs feed on dead leaf material and detritus in the colony.

Dung is a useful natural resource; it’s readily available and versatile, but as is clear, there is one predominant use – as a foodstuff for all the scavengers that come along later. From now on, this book will concentrate on the key fact that animal dung still contains very high levels of usable nutrients, and that these are particularly attractive to insects – dung beetles and dung flies. One way of thinking about this is to follow their philosophy, and to regard dung simply as pre-owned food.

¹ Someone is going to ask, so for their benefit: Onthophagus coenobita, O. similis, Aphodius ater, A. equestris, A. erraticus, A. prodromus, A. pusillus, Sphaeridium scarabaeoides. Also the predatory rove beetle Ontholestes murinus.

² In a similar extreme association, the minute specimens of Acuminiseta pallidicornis (lesser dung fly family Sphaeroceridae) ride around on the backs of giant African millipedes in the jungles of West Cameroon, waiting for their hosts to deposit large (to the fly), invitingly moist frass droppings (Disney, 1974).