Call of Nature: The Secret Life of Dung

D ESPITE THE SEEMINGLY mad free-for-all of new arrivals at a freshly deposited cow pat or horse dropping (or extruded stool), there is method in the insect madness, actually several methods. These are the various strategies that have evolved in beetles and flies (and a few other animals) to make sure they are successful in carving up just enough of the dung to get their offspring through to the next generation.

As was noted in the previous chapter, the first arrivers get a good start. And despite the early beetle appearances at my small private experiment around the back of the recycling centre near Reading, flies, by virtue of being good at flying, are often the very first to land. Indeed the horn fly, Haematobia irritans, is recorded laying its eggs in cow dung before defecation has finished. This is a rather risky business. Anyone who has ever witnessed cow dung coming into the world will know that its liquid texture means it is, quite literally, squirted down and splattered up. Being in the air near such a torrent is fraught with danger, and the small fly must calculate its trajectory and be aware of airborne droplets with expert precision if it is to dip down, lay its eggs and make its escape safely. It also uses horse dung, the drier boluses of which are, perhaps, less likely to splash, but which can still damage an overly keen insect unless it keeps a watchful eye on what is falling where.

The horn fly larvae are equally hasty; they hatch within hours and start feeding immediately. Within about 7 days they have devoured enough to pupate, ready to change into adults. They are still, however, in danger from predators, and must wriggle away from the pat to hide in the surrounding grass root thatch, but at least they have successfully taken their fill of the scarce dung resource.

The yellow dung fly, Scathophaga stercoraria, is equally keen; in case we were in any doubt its scientific name means ‘dung-eating dung-dweller’, and it lives up to this by arriving on site seconds after the deposit has been made. These bright orange-yellow fluffy flies are not egg-laying, though, they are the males. They know the females will be along soon, but they are invariably first on the scene to carve out territories. Waiting for the slightly smaller, more demure, greenish-grey females to appear, there is a certain amount of aggressive posturing amongst the males. Like so many insects, larval foodstuffs and adult tastes differ widely; whilst the larvae may be dung feeders, the adult flies are ferocious predators, and they are not above using their powerful grasping legs and stout spiked mouthparts on each other in the mêlée. There is a tension in the air as a fresh pat 30 cm across may have 20–50 alert male dung flies each vying for its own precious few square centimetres of glistening faecal surface.

Fig. 18 Despite its bright pelt of hairs, the yellow dung fly avoids getting mired in the gloop.

A ratio of four or five males to each female means that there is no such thing as a dung fly wallflower. The dearth of females may be because they are not able to mate straight after emerging as an adult; they spend 2–3 weeks maturing, catching and eating small flies and other insects to give them a protein boost in preparation for the arduous body-depleting business of laying eggs. The males, however, are ready to go much sooner. As each egg-ready female arrives at the pat, there is an undignified scramble. The nearest male grabs her and mates without anything in the way of courtship. A second or even a third male may pounce too, attempting to wrestle the female away from her first suitor, even if coitus is underway. Such is the competition for females that the successful male clings to his trophy wife when sperm transfer is complete to prevent the female mating again. Female dung flies can mate several times, but it is in the male’s interests to hold on as long as possible, preventing latecomers intervening, thus diluting his sperm and reducing the number of his offspring amongst the eggs she lays. The female also gets some benefit from her protective partner, since constant pestering attempts by other males, desperate to mate with her, can cause physical injury to her delicate body. Still mounted on her back, he will stay in attendance as she lays her eggs in the dung. It is only as the last egg of the batch is laid, which the female signals with a sashay of her body, that the male finally relinquishes his hold and flies back onto the dung to await a new female arrival. Meanwhile the female flies off to feed on nectar and insect prey whilst she matures a new egg batch in her abdomen ready for another tussle on another cow pat in a few days’ time.

The ease with which these flies can be observed on their pats, males and females easily distinguished, numbers counted, liaisons monitored and timed, egg batches measured, and paternity rates calculated, has lifted Scathophaga stercoraria to the status of model biological system. Scientific papers reporting on its behaviour, genetics, nutritional ecology and life history have burgeoned since G.A. Parker (1970) first took up the study. We now know quite a lot about the yellow dung fly; we can experimentally interfere with its life history and we can make quite precise calculations about its behaviour.

For example, as a fresh pat becomes crowded with males, the chances of a newly arriving male grabbing an incoming female falls, and it might pay a slightly late male to hang around in the nearby herbage, trying to intercept a female, rather than waiting in the main arena with all those other desperate competitors. There may be fewer females here, but this is offset by there also being fewer competing males. Very pleasingly the observed numbers almost precisely match the predicted numbers, with a large number of males on the dung itself, but the majority in the 20 cm zone of grass nearest to the dung, then numbers dropping off as they get further away (20–40, 40–60 and 60–80 cm zones).

Optimum mating and guarding times can also be calculated. It takes roughly 2.5 hours for any individual male to go through the whole process of finding a female, mating with her and standing guard whilst she lays her eggs. Given that the female may have mated previously, and still be storing some sperm in the storage duct (spermatheca) in her abdomen, the male needs to maximise his own sperm usage for her next batch of eggs. But the longer he spends inseminating her, the longer he puts off her actual egg-laying session, and the less time he will have to go off on his next romantic jaunt. The mechanics of fly sperm transfer can be measured by deliberately interrupting mating pairs at various times and seeing what proportion of the eggs are fertilised. It soon transpires that once a male can ensure 80% egg fertilisation with his genetic material, there is little to be gained from further effort – a neat example, from life, of the law of diminishing returns. This, then is the optimum time to stop mating and start guarding, so the female can offload her eggs, at least the majority of which he will be father to. The predicted time is 41 minutes of coitus and the observed time is 36 minutes; you don’t often get such close agreement in biological experiments.

In my first year of university (1977), the week-long ecology field trip to Ashdown Forest had us studying birch invasion rates over heathland, the numbers of case-bearing amoebae living in the sphagnum moss, and measuring the arrival, mating, guarding and egg-laying times of cuddly dung flies as we lay belly down in a grazing meadow, closely observing fresh and fragrant cow droppings. Ah, such fond memories.

Scathophaga eggs are laid on the surface of the dung, in a crack or under the overhang of a wrinkle, but as soon as the larvae hatch they burrow down into the dung. For all dung-feeding fly larvae, speed is of the essence. Maggots are soft and vulnerable, easily attacked and eaten by other creatures (who’ll be making their attack later on in this chapter), so they rely on being hidden in the dropping while they get on feeding as quickly as possible. Scathophaga takes about 3–4 weeks from freshly laid egg to newly emerged adult. Females emerge a day or so before the males, but need to spend another 3 weeks, feeding at flowers and eating small insect prey, before they are sexually mature. Sperm being easier to manufacture than eggs, the males only require about 1 week of predation before they are ready to mate.

Other flies are equally eager to get through the dangerous larval stage as quickly as possible. In many of the smaller dung flies (families Muscidae, Sphaeroceridae, Sepsidae, etc.) larvae have finished development in under 2 days, and a complete life cycle takes just over a week.

Even at this speed, though, competition is still strong; an early start does not guarantee enough food if everyone else starts early too. Just as with dung beetles, there is considerable size variation in dung flies, and if there is just not enough food to go round, a larva will take the gamble of becoming a small pupa, then a small adult, rather than waste time searching out leftover morsels in the surrounding soil. In laboratory studies of the common (and annoying) face fly, Musca autumnalis, larval densities were artificially manipulated and a threshold of 5 mg dry weight of dung was measured below which pupal and adult size fell away sharply.

Flies may be the flighty ones, getting in quick and racing through development as quickly as possible, but leave it to the dung beetles, the true masters of the faecal environment, to invent the most diverse series of fascinating behaviours to get around the constant problems of inter- and intra-specific competition. My personal beetle bias is going to come to the fore again here: although I will keep trying to introduce other groups, I maintain that a natural history of dung is really a natural history of dung beetles, and in particular those in the superfamily Scarabaeoidea. Others are with me on this, and there have been a series of hugely important ecological monographs in the last 25 years, notably those edited by Hanski and Cambefort (1991), Scholtz et al. (2009) and Simmons and Ridsdill-Smith (2011a); though highly technical and immensely detailed, they are a mine of information, and I have delved deep.

The Scarabaeoidea is a large group of attractive chunky beetles; it also includes the stag beetles (astonishing beasts) and the chafers (some of the most brightly coloured and beautiful insects on the planet). Dung beetles have long held a fascination for entomologists. Dutch naturalist Jan Swammerdam, writing his Historia Insectorum Generalis in 1669, enthuses of the two he had come across: ‘One of them is conspicuous by a purplish gloss, like that of copper, on its breast and belly; the other glitters like green molten brass or copper delicately gilt, and indeed makes a very beautiful figure’ (from the English translation, 1758). I hope my understandable fondness for them will be indulged. We know a lot about scarabaeid dung beetles; originally their relatively large size and attractive body forms made them popular to study (all those weird horns helped), they were easy to find (just look for a dung pat), and they carried out the seemingly driven, thoughtful, calculated behaviours of digging holes, excavating tunnels, burying dung and playing with balls of the stuff.

Once we get over the sheer amazement of just what these dung beetles are doing, the question soon arises: why? The answer to this question is now a vast field of entomological endeavour. The evolution of many of these behaviours appears to have been driven by the biological success of parental care, particularly in the complex procedures of making a nest. Most insects have no truck with parental care; large numbers of eggs are simply dumped somewhere and offspring are left to fend as best they can in the bug-eat-bug world out there. Thus, any parental care systems in insects are bound to attract the attention of biologists, not least because of their novelty. Parental care, and/or nesting, can really only work with manageable (i.e. small) numbers of offspring. On the whole, dung beetles rear relatively few young, sometimes only one at a time. Nevertheless, the idea of dung beetles working to build a nest home in the putrid morass of the animal dropping might, at first, seem an unlikely suggestion; however, there are genuine analogies between nesting dung beetles and the better-known nesting behaviours of birds and mammals. A nest does not need to be an elaborate construction built of leaves, twigs, mud daubs, or other collected biological or inorganic debris. It can simply mean a hole (e.g. woodpeckers), a scrape (hares) or a tunnel (badger), or simply a small corner made one’s own. The key attribute is that there is some sort of provisioning, either in terms of food, nesting material, insulation, security or protection from the weather. Now a nest in the dung sounds a bit more plausible.

Fig. 19 Typical central European dung beetle diversity, from Reitter (1908–1916).

It’s all to do with reproductive pay-offs in terms of construction effort and the number of offspring successfully surviving. Without going into too much complexity here, it’s enough to know that mathematical models can be designed to demonstrate how various behavioural strategies lead to various outcomes in terms of clutch size and number of offspring. There are several possibilities: (a) both parents can desert, the non-nesting strategy typical of most insects; (b) the male cares exclusively (rare, but does happen in a few birds and mammals); (c) the female cares exclusively (perhaps the most common, especially in ‘higher’ animals); (d) both parents care together. That last option is the one familiar to anybody watching a pair of birds working in concert to build a nest, lay and hatch eggs, then feed the constantly open craws of the hatchlings. Surprisingly this is also a common parental care strategy of many dung beetles.

Not all things are equal though. Traditionally, males and female animals are seen as having a different commitment to their offspring. The female, with a relatively huge egg investment, contrasts with the male’s easy and copious sperm offering. An obvious male strategy is to mate with as many females as possible in the hope of siring as many offspring as possible. This is the tactic of those hornless minor males. This is all very well, but it immediately leads to sperm competition and dilution effects, and the possibility that, in the end, only a few males ever get to father anything. As with the dung flies, staying with a mate, and guarding her, can be the better option.

An important biological concept here (a central tenet of the trivial-sounding, but mathematically robust, ‘game theory’) is that parental behaviours evolve because of what is happening in the majority of the population, not necessarily in every individual. Infidelity and desertion may still occur, and strategies may change if circumstances change. There is room for behavioural plasticity. In the scientific jargon, an evolutionary stable strategy for biparental care can occur if the success of both parents working together is mostly twice that of one parent working alone. In simplistic terms, and slightly patronising tone, the family is greater than the sum of the individual parents.

In birds and mammals female-only care is very frequent, and in birds there are occasional examples of male-only care. In dung beetles a lone female can rear her own offspring, but since most of the ‘care’ is in the provision of a brood ball, before egg-laying, a male can only do so much on his own – he can’t lay the necessary egg; male and female working together is the dung beetle brood-care norm.

Because dung beetles are easier to rear, easier to observe, and less ethically challenging to interfere with, they are now important biological models for testing nesting theories. Move over dung fly mate-guarding experiments, the beetles are here.

One easy measurement to come up with is the fact that the amount of dung set aside as a brood mass by the mother has a direct influence on the size and emergence of the offspring. Experimental manipulation of a brood mass, removing or adding material, is relatively easy. As is the measurement of any extra help in this, given by the male. Using offspring body size and male horn length as a good measure of larval nutrition, only the very largest females can rear handsome horn-toting major sons if they are working alone; but when a male helps, even the smallest mothers can produce majors. They are so proud. Interestingly, paternal help does not increase the number of brood masses (with one egg in each); this is limited by a finite number of eggs in the female’s ovaries. Thus, male help does not increase the number of offspring, it increases their size and strength – their fitness in Darwinian terms of best being able to pass on their genes (half of which are his) to the next generation.

Broadly, there are three main nesting strategies for dung beetles (that’s the large families Scarabaeidae, Aphodiidae and Geotrupidae again) using dung, and these all boil down to how the adult beetles deal with the dung when they arrive so they can best provision a nest, or at least secure a food store, for their grubs.

The most dramatic, the most obvious and the most often seen in wildlife films are the rollers – the telecoprids (from the Greek, more or less meaning long-distance dungers). These are the beetles which cut away a chunk of the pat, shape it into a ball and roll it away to bury it some way off. The ancient Egyptians revered the sacred scarab for this amazing behaviour, and it is similar species which are partly responsible for the wild frenzy when it comes to reducing a huge elephant dropping to meagre remains.

Next are the tunnellers – the paracoprids (more Greek, meaning beside, near or against the dung). They dig their burrows underneath the pat, or immediately adjacent to it, and drag balls, boluses, nuggets or pellets down into the soil, making small accumulations at the ends of the tunnel or in blind side-burrows. These beetles tend to work unobserved, but because of their head-to-head face-offs in the subterranean workings these are the species that have evolved the sometimes enormous, sometimes bizarre, head horns and thoracic horns.

Fig. 20 Bold and stout, Aphodius fossor.

Lastly there are the dwellers – the endocoprids (obviously meaning insider dungsters). Some of these just crawl or burrow into the dropping, chewing out or shaping voids, but not really doing much in the way of apportioning or concealing dung for the special use of their own offspring. Others gather a parcel of the dung and shape it into a discrete brood ball within the greater dung mass.

Taking these in reverse order, we’ll start at the most fundamental dung–beetle interaction – the beetle just arrives at the dung and feeds on it, or lays its eggs in it. Arguably this is the most evolutionarily basic starting point for the complexities of nesting behaviour.

OK, I’m going to backtrack a bit here because in northern Europe the majority of true dung beetles are dwellers, but not necessarily nesters. The hugely diverse family Aphodiidae, mostly members of the genus Aphodius, are the majority stakeholders here. There are around 1,650 worldwide species in the genus, they tend to be smaller, narrower and more cylindrical than the other major groups, and they don’t really make nests.

The aphodiids dominate dung in northern temperate zones. Even in Britain we have 55 species (compared to 15 tunnellers and no rollers), and of these, 15 species can be living together in the same cow pat or horse dropping – though the most I’ve ever found is 12. It seems they live a more leisurely life, and that here at least, they do not need to take part in the undignified scramble for possession. There is enough dung to go round, it does not dry out too fast in the cooler, damper climate, and anyway they are happy enough with slightly stale dung. They are mostly small – Aphodius fossor, at up to 12 mm, is the biggest, but most are below 7 mm – and they have adapted to the meagre and well-scattered droppings of deer, rabbits and the occasional entomologist obeying the call of nature. They tend to push underneath the dung, from the side, and will either burrow into the mass, hollow out small cavities or live underneath the pat. Here most lead an itinerant life, with little or no social interaction, and with scarcely anything that could be considered nesting behaviour.

Other dwellers, such as the scarabaeid Oniticellus (six Eurasian species), are less indolent. Although they remain in the centre of the dung pat, they actively shape portions into individual brood balls and lay their eggs in them. In true nesting spirit they may even remain on site to guard and monitor their developing offspring. Exactly where one brood ball begins and the dung mass ends is sometimes difficult to interpret, but some dwellers seem on the cusp of evolving more advanced nesting behaviour. The common Aphodius erraticus digs a shallow depression into the soil 3–5 cm deep, barely worth being called a tunnel, directly under the dung, and fills this with morsels of dung after laying an egg at the bottom. Elsewhere Aphodius luridus lays its eggs at the dung–soil interface and the larvae dig themselves short rudimentary tunnels into the soil which fill up with dung-infused liquid sludge every time it rains or there is a heavy dew.

As well as the ‘true’ dung beetles above, there are plenty of other dung-feeders from different beetle groups that also just feed inside the general dung mass. Some of these will be visited in chapter 6. Nesting is not shown by any of these other dung-dwellers, but it’s important to remember that they and lots of other organisms are part of the scramble for possession, and it is this that has led to the evolution of slightly more complex brood-care behaviours.

The shovel-headed bulldozer-like form of the broad scarabaeid and geotrupid dung beetles couldn’t be better designed for moving earth. They immediately set to work digging down into the soil, either right under the dung, or with an entrance close beside it. How far they dig down depends on the beetle’s size and the soil type.

When, as a 14-year-old schoolboy, I helped out at an archaeological dig on the South Downs behind my parents’ Newhaven home, we cut away the turf in rolls, and removed the meagre few centimetres of topsoil, looking for Iron Age post-holes in the underlying chalk just beneath the surface. We regularly found the duck-egg sized brood balls of dor beetles (Geotrupes species), 10–15 cm down; that was as far as they could go, before they met the impenetrable limestone bedrock. On the other hand I knew not to bother trying to unearth the minotaur beetle (Typhaeus typhoeus), which in the loose greensands of Ashdown Forest could easily penetrate more than a metre down.

It’s not the kind of crass fact that dung beetle researchers like to brag about, but I’ve had a brief scour of the literature to find the deepest recorded dung beetle tunnel. The best I can offer is a North American species – the aptly named Florida deepdigger scarab, Peltotrupes profundus, with a burrow recorded by Henry Howden (1952) down at least 9 feet (2.7 m). There are just two caveats here. First, it seems that P. profundus, though obviously a dung beetle (family Geotrupidae), is not necessarily a dung-feeder, but a general soil humus and leaf litter detritivore; the non-dung foodstuff of some species is an important consideration when examining the evolution to and from coprophagy in chapter 7. Secondly, someone out there is bound to know of a deeper digger, so if they let me know there may be further updates in a second edition of this book.

Fig. 21 Only the male of the minotaur beetle, Typhaeus typhoeus, has the three strong thoracic horns.

Fig. 23 Onthophagus bifasciatus, an Indian and Central Asian species.

Most tunneller burrows are of the order of 20–100 cm deep. The obvious point of burrowing is to get a portion of the dung out and away from potential competitors quickly so that it can be put to the sole use of one beetle; or a pair of beetles. Away from the mad scrambles on tropical savannahs, where hundreds or thousands of beetles jostle, but then each end up with precious little to their name, tunnellers can be the big-time winners. A pair of large tunnellers can easily bury 500 g of dung under a pat, so these beetles make a powerful contribution to dung removal from grazing pastures.

There is no hard and fast rule, but very often a male and female meet at the dung patch, form a short-lasting bond and work together to build a nest. Each species will have its own strategy for where, how deep and how often it digs its nests. Here is where game theory predictions of paternal assistance and laboratory measurements of brood ball size come together.

Fig. 22 Male and female Copris lunaris work together to raise a faimly.

As ever, in nature, there is often a trade-off between effort and results. The deepest and longest tunnels may be the safest, but they take time to build, and if the dung supply is limited it may be gone before an elaborate subterranean chamber can be constructed; or the beetles may only get one chance at it. A series of short tunnels can be dug fast, and stocked quickly with the diminishing dung, but they may not be far enough out of the way to escape interference and disturbance from all the other frantic diggers. Each dung beetle species adopts its own nesting strategy.

At its simplest, a female makes a rudimentary tunnel, sometimes just a vague depression, right underneath the pat; she buries a clump of dung, lays an egg and leaves it to get on with another one. This is the lowest-maintenance option, quick and easy for a female working alone, but still very basic. She will hope to have at least some offspring success through the larger numbers of eggs she releases, 10–50 per pat, maybe 130–150 in her lifetime. In other species a slightly larger hole is filled with several brood balls, all more or less touching each other, each with its own egg. There is less time digging, but this is still an easy option for beetles laying higher numbers of eggs.

Deeper tunnels are usually made in the species where males actively assist. These can be simple tubes, with a series of 5–15 brood balls, or sausages, wedged in at irregular intervals near the bottom. Like those produced by the minotaur beetle (Typhaeus), they may be quite deep, up to 1.5 m. The tunnel is dug first, then morsels of dung are brought down and packed around the egg. Subsequent eggs are laid in other balls as the beetles work back up from the deepest part of the shaft. Or the shafts may branch (an approach favoured by many Onthophagus and Onitis species), culminating in groups of short cells, into which the round dung balls are placed individually or in small clumps. At this level of sophistication one or both sexes may stay in the tunnel, guarding the brood.

The most complex tunnel-nesting behaviour is shown in a very few of the larger species. The ‘English’ scarab, Copris lunaris, and its congeners, are good examples. Each tunnel is dug by the male-and-female pair and a small number (2–10) of large roundish balls of packed dung are created by bringing it down piecemeal and shaping it in the nest void. Each spheroid ball receives a single egg just inside one end. The nest chamber is large enough to accommodate all the brood balls, keeping them separate, and at least one parent (usually the female) remains in the nest, protecting and tending the developing grubs inside their spherical golfball-sized pods. She keeps the pods upright in the nest, and repairs them if they break open whilst the larva is developing inside. If a female is removed from the brood chamber, fungus soon develops on the dung balls. It is only when the larvae have achieved pupation, or are at least well into their larvahoods, that the adult beetle will move off to find another dung source and try to repeat the process. An adult female beetle may only live a year or two, and can only produce 10–30 eggs over her lifetime, so she invests whatever is necessary to give them the best chance of success.

Fig. 24 Rollers hard at work, one of the Detmold paintings inspired by Fabre’s works.

Ball-rolling dung beetles show some of the most complex and fascinating behaviours anywhere in the insect world. It’s no wonder that they inspired the ancient Egyptians to revere them, and to incorporate them into a complex other-world system of bizarre animal deities. At least one entomologist (Sajo 1910 quoted by Hogue 1983) has suggested that the biblical account of Ezekiel’s wheels (Ezekiel 1:1–28) was a mystical allusion to roller scarabs, and not some new form of four-winged shining-bodied cherubim, nor alien astronauts.¹ Sadly, such rollers do not occur in Britain or northern Europe, but the original sacred scarab, Scarabaeus sacer, occurs in southern France, and was the inspiration for French entomologist J. Henri Fabre to write about the sacred beetle (1897). Coleopterists have been hooked ever since.

The ball is initiated by an ‘active’ partner; in Scarabaeus and Canthon, this is the male (but in other genera, e.g. Gymnopleurus, Sisyphus, Phanaeus, it may be the female). It may take a few minutes, to up to an hour, to scoop, shape and sculpt the ball, which is rolled only a short distance away at first. This initial ball may act as an attractant, bringing in a female to feed. Having travelled in some distance, possibly from her last nesting job, she will be hungry, in need of that ever so important dung soup to replace lost nutrients and replenish her ovaries. She is attracted by the dung, but is even more attracted by someone telling her they’ve got the dinner ready. In the closely related African genus Kheper, the male disports himself on the ball he has made; balancing head down, tail up at an angle of 45°, he releases a sex pheromone by striking his legs against abdominal glands, sending puffs of white powder, containing the scent, into the air (Tribe and Burger 2011). This is a clear indication to the female that a potential mate has made a head-start; she may feed on the dung ball, or get straight on with the business of putting it into a nest.

When the ‘passive’ partner arrives, there may be some jostling, or she may be accepted immediately. There are few reports of anything that can be considered courtship, but it has been suggested that unequally size-matched beetles often fail to pair up. This may be because rolling a dung ball is easier for two equivalent beetles, rather than large and small struggling awkwardly together, like Laurel and Hardy moving that piano.

To roll a heavy dung ball, a dung beetle stands, head-down, on its front legs, and uses its long middle legs, and very long hind legs, to control the ball, as it pushes backwards, off and away. It is not just casually ambling along, easily trundling a smooth marble, but maintains a careful grip on the ball. If it tumbles it tries to keep hold, picks itself up and sets off again. In an odd departure from normal beetle anatomy, members of the genus Scarabaeus do not have front feet. The front legs, on which they push down onto the ground when rolling, lack tarsal segments and claws; however, the middle and hind legs have normal five-segmented tarsi and the usual double claw to maintain a grip on their sometimes wayward cargo.

As with tunnellers, there are various options as to how rollers manage their dung-removal strategy. Despite the obvious benefits of pair-bonding cooperation (after all, a dung ball can be 50 times as heavy as each individual beetle), there are rare instances of a female working alone. It is only regularly known in one species, Megathoposoma candezei, from Central America, the only instance of a roller operating without any male help ever. After mating near the dropping, the female sculpts out a ball of dung and rolls it away on her own, to bury it and lay her eggs.

The most common behaviour is for male and female to work together at the dung face. The female may spend more time shaping the ball, but the male is the powerhouse when it comes to rolling it away. They bury it a few centimetres below the soil surface, then mate. At this point they separate and the female works the brood ball into an egg or pear shape, maybe two. She lays an egg in the narrow upper end of each dung ball and leaves the nest to repeat the process, sometimes with the same male, if he is still about, sometimes with a new suitor. There is some variation to this behaviour. Some species of Neosisyphus have very long legs and may roll the dung well out of reach of other competitors, but they do not bury the brood ball; instead they leave it attached to grass stems or twigs. This might save on time and energy, but risks desiccation and predation of the developing grub inside.

Further up the ladder of sophistication, Kheper females remain in the nest with the brood ball. The original rolled dung ball is reshaped into one or more (up to four, depending on the species) pear-shaped masses and each is inoculated with an egg. The mother then stays with her offspring until they emerge a month later. This is intense maternal care, and because of the seasonal movement of grazing animals, and the seasonal moisture content (or rock hardness of the soil), she may be limited to rearing only one offspring per season, and frequently only one per year.

Alternatively the bonded pair of beetles may return to the food source and bring further balls back to the nest. Eventually, when it is fully stocked, the female (sometimes the male too) remains in the nest looking after the brood, some species remaining in their nest until the new beetles emerge.

One intriguing aspect of brood ball nesting behaviour is that a grub feeding inside the bolus not only has a limited amount of food at its disposal, but is literally living inside its own food. This means it must defecate inside its own food too. As it feeds on the inside of the dung ball, it grazes out a spherical hole just a fraction larger than its fat, curled, C-shaped body. As it grows it must add its own frass back into the ball. By the time the larva is fully grown, it has eaten almost the entire contents of the ball, leaving just a thin shell 3–4 mm thick. This means that the larvae has ingested and reingested its own faeces many times over. This may be analogous to the caecotrophy shown by rabbits re-eating their night faeces.

The nesting behaviour itself is fascinating, but it is the rolling of dung balls that has captured the imagination of ancient philosophers and modern scientists alike. One of the most obvious things is that a roller (or a pair working together) do not just trundle off at random – they plot a trajectory and stick to it. In other words they set off from the dung in a straight line, and persevere no matter what gets in the way. If they meet an impenetrable and insuperable barrier, they may have to adjust direction for a short while, but as soon as they find a gap, or the end of the barricade, they resume their original heading. This doesn’t necessarily mean that they are heading for a known final destination; that would require some backtracking triangulation when the way was clear again. Instead they are maintaining a fixed course, taking them away from the dung, away from competitors, as quickly and as directly as possible. There is no predetermined or favoured direction; mapping rollers moving away from the pat shows them radiating out to all points of the compass, but they are all moving in individual direct straight lines. They do this by using the sun.

Fig. 25 Condemned by Zeus to push a boulder forever uphill, Sisyphus, king of Ephyra, gave his name to a long-legged roller, beautifully depicted here by Detmold for Fabre’s Book of Insects (1921).

There are some simple tricks to demonstrate this. Blocking the sun with a board, and using a mirror, moves the sun’s apparent position in the sky, and the roller, striding out in mid-journey, quickly recalculates and reorients itself accordingly, unaware that it has been misled, and tricked into making an angle change. Conversely, gluing a small cap to the beetle’s thorax, so that the eyes are covered, has them rolling their balls round in aimless circles and directionless spirals.

Dung beetles, like many insects (honeybees for instance) not only see light and shadow, and perhaps some colours, but they can tell the direction of the light as it passes through the air – they can measure its polarisation. Even if the sun is obscured by clouds, they can tell where it is, not by the relative brightness in the sky, but by the angle at which light strikes their eyes, something that we, as even very visually adapted humans, are incapable of doing.

The large African Scarabaeus zambesianus forages at dusk, and even though the sun is no longer in the sky it can detect light polarisation in the atmosphere, though human eyes struggle to make out anything in the gloom beyond a few dark blobs jostling in the dung. The uppermost dorsal ridge of its eyes contains huge light-sensitive cells, much longer and wider than in any of its day-rolling contemporaries. It is these which detect, not just much lower light intensities, but from which direction the light originated (i.e. where the sun is below the horizon). Looming over the roller’s twilight perambulation with a large polarising filter, its axis set perpendicular to the recently set sun, immediately makes the beetle turn 90° left or right, realigning itself so that it thinks it is maintaining the same course. As it moves out from under the filter it rediscovers the sky’s true polarisation pattern and reverts to its original trajectory. Entomologists are full of these experiments to tease the beetles.

Being active at night helps S. zambesianus avoid competition with much larger rollers such as Kheper, and on about 180 days of the year it can extend its foraging well into the night using the disc of the moon. Its visual acuity is so good that even if it cannot quite make out the pearly body of our celestial satellite, it can still detect the polarisation pattern, though this is less than one-millionth that of the sun.

Perhaps it should come as no surprise that dung beetles also use the stars to navigate. Marie Dacke and colleagues (2013) glued those same small caps over the heads of South African Scarabaeus satyrus and released them into a shrouded arena to roll their dung balls away as quickly as possible. They found that, on moonless nights, the light from the Milky Way was enough to guide the beetles. There is no suggestion that the beetles were navigating in the same way early pre-compass mariners used individual stars or constellations, but the diffuse band of pale light from the Milky Way did register, an observation confirmed in a similar arena set up in the Johannesburg Planetarium, thanks to assistance from the obviously patient and tolerant staff there. The latest suggestion is that the beetles, whether rolling by day or by night, take a visual snapshot of the sky, creating a mental picture of light intensities, polarisation, and position of the sun and/or moon, and use this stored mental image to compare to the physical world as they roll along (el Jundi et al. in press).

Whether travelling by day or by night, 20 minutes is an average ball-rolling time, allowing the beetle to get about 15 m away. The further it gets from the original pat, the safer it might feel about the food security of its offspring, or itself.

At this point I find myself slightly disappointed that nobody appears to have done a fastest-dung-roller Olympic speed trial. Again, perhaps that’s not quite the done thing in a deeply serious scientific monograph. Anyway, I’d like to suggest the African species Pachysoma gariepinum, which charges around the Namib Desert at 0.33 m/s. That’s a very respectable 1.2 km/h (about 4 mph), and at least twice the speed of your average sacred roller. It probably does this to avoid burning its toes on the scorching sand of the desert’s notoriously furious dunes.

Pachysoma is a bit of an oddity. It has no wings, and cannot fly. Indeed its wing cases are fused together down its back – an adaptation to avoid excessive water loss in this, one of the driest places on the planet. It gathers bits of dried dung and other detritus from the shifting dunes, making erratic wandering exploratory meanderings until it finds something to scavenge; then it makes a beeline back to its nest. It drags its booty behind it, instead of rolling it up front. Rather than setting off in a straight line from a large dung mass to bury its treasure far away from competitors, it ekes out a living in a bleak landscape, surviving only at low density, where really its only competition is with the fierce climate (Scholtz et al. 2004). What little it finds, it has to accumulate back at a base-camp, so it must somehow make a mental map of its immediate surroundings, presumably using rocks or clumps of dead scrub as landmarks to aid navigation back home.

Fig. 26 Scarabaeus sacer, one of the largest, most powerful and most familiar of the large Old World scarabs.

Fighting is perfectly natural. It is, after all, a matter of life and death, at least for any potential offspring, whether a mate is wooed, a food is found, prey is caught, nest sites are secured or a big enough bolus of animal faeces can be assured. Fighting, or at least the threat of it, gave rise to those ridiculous horns in many tunnelling dung beetles. Subterranean contests go on, and there is usually a victor and a vanquished; very often it is sheer body size or horn length that determines this.

Rollers try and get their stash of dung as far away as possible, as quickly as possible: theft of dung balls is rife in the treacherous low-life neighbourhood of the dung pat. There are about 1,000 species of dung-roller beetle in the world, but in any given geographical location there is unlikely to be more than 10 (maximum 20) species. This is because competition is so intense that after massive squabbling there may not be enough for any single beetle to make one ball. Most of those thousands of dung beetles reducing an elephant dropping to nothing probably went off empty-footed. Speed may be of the essence, but so too is targeting a particular part of the day (or night), concentrating on a wetter or drier habitat, timing emergence to a different part of the season, or growing larger or smaller.

This last consideration is important, because size very often means might, and in nature might often ends up on top. On top of the dung sphere, a fighter will try to defend (usually) his ball against any other beetles trying to steal it. However, it is not worth a large roller stealing the insignificant ball of a small roller; it simply will not be big enough to rear a grub. This is good for diminutive species which might otherwise be the victim of much larger bullies. Fights usually occur between well-matched individuals, often of the same species. Both beetles grasp the dung ball and try to wrest it from the other’s grip by making sudden flicking movements with their powerful front legs. In Kheper they might resort to head-butting and thrashing each other with their broad, spiked, front legs. Occasionally they will grapple together bodily, the loser eventually being tossed aside, literally thrown up to 10 cm away. The flattened front of the head, the clypeus, is used a bit like a frying pan tossing a pancake. Generally the larger beetle (whether the same or a different species) will win out and in a neat laboratory stadium experiment, nine diurnal and seven nocturnal species from Panama (Young 1978) showed a linear size hierarchy. In fight manipulations with Kheper, winners were on average 10% heavier than losers.

Occasionally contests involving three species are reported, when Jean-Pierre Lumaret observed Scarabaeus typhon make a dung ball in Corsica, it first had to fend off a similar-sized specimen of S. sacer; it was subsequently challenged by S. laticollis and the same individual of S. sacer returned for a three-way brawl. In the event, the original S. typhon remained the owner. A rightful owner retaining the ball seems the usual outcome in equally matched fights, the ball creator manoeuvring itself between the dung and the attacker, whilst continuing to roll the ball away.

Muscular power is not just linked to size, but is also related to body temperature. Dung beetles, like all insects, are poikilothermic (what used to be called cold-blooded): they cannot readily control their internal temperature (unlike you and me, homoeotherms). Mostly this means that a beetle’s internal body temperature is only a degree or so above ambient, so insects have to wait until the day warms up before they can get going. Some bask in the sun, but they are very much at the mercy of local weather conditions. In the cool morning, when large elephant droppings are usually dropped, dung beetles need to overcome any dawn sluggishness, and get warm enough for active flight – around 34°C. Larger beetles can do this by shivering. This involves rapidly vibrating the internal flight muscles, without actually flapping their wings, generating physiological heat in the musculature. This raised body heat not only helps the beetles get to the dung pile in the first place, but also assists them should any conflict arise. As well as significantly larger Kheper beetles most often winning experimentally manipulated ball fights, so too hot beetles (average thorax temperature 38.7°C) tend to win over cooler ones (average 35.2°C). They’re all pumped up and ready to rumble (Heinrich and Bartholomew 1979a). It doesn’t always work out though. Staging test fights between large African rollers often resulted in the dung ball being torn apart in the frantic vigour of the contest. The evil scientists had to trick the beetles into fighting over artificial balls made of clay, impregnated with elephant dung juice. Rotters.

A warm beetle is also a fast beetle, so a large Kheper laevistriatus hot from its flight to the dung is quicker at sculpting the brood ball, and faster on the off as it makes a dash to bury it. The time required for a beetle 25 mm long to build a dung ball the size of a tennis ball can vary from just over 1 minute to nearly an hour. On level ground, roll rates of 14 m/min have been recorded by hot (>40°C) beetles; by the time they have cooled to 32°C they were dawdling at only 4.8 m/min. Back in the Namibian death dunes, though, speedy Pachysoma gariepinum can easily outpace anything else foolish enough to venture under the midday sun.

Sadly, the beetle equivalent of bringing home the bacon and securing it in the larder does not necessarily stop widespread pilfering. Just as minor hornless males can sidle past their well-endowed major competitors to sneak-mate with the females, so too nest parasites can take advantage of another beetle’s buried dung store and sneak in to lay their own eggs. This cuckoo parasitism is, like the bird that inspired the term, a genuine usurpation of the host’s hard work and often results in the host grub’s death in favour of the kleptoparasite (from the Greek κλεπτες, kleptes, ‘a thief’).

Amongst the dwellers, where no very clear nesting or brood ball creation is visible, it is difficult to distinguish between a true kleptoparasite and an interloper just burrowing over to pinch a bit of dung. In Britain, for example, species of the large genus Aphodius seem to inhabit just the pat, feeding on their bit as best they can. There are a few reports that the large and common A. rufipes can be a cuckoo parasite in the buried brood balls of the large dor beetle Geotrupes spiniger, whilst the small rare A. porcus has (once? Chapman, 1869) been found in the nests of G. stercorarius. Both, however, can also be found above ground simply ‘in dung’. This suggests that kleptoparasitism is not a necessary part of these beetles’ life cycles, but that if they find dung buried by some other beetle, they will take advantage.

Away from the temperate northlands, tunnellers and rollers abound; here cuckoo parasitism is more often reported, and we can make better assertions that some species are genuinely adapted to the parasitic lifestyle. In some places 10% of all dung beetle species are kleptoparasites. A single nest of the large tunneller Heliocopris antenor contained 130 specimens of ten other dung beetle species, although six of these (four species) were thought to be non-parasites which had just been caught up in the tunneller’s zeal and buried accidentally in the large dung mass. Even the rollers can’t get away from them: one large Neosisyphus ball contained 37 individuals of six cuckoo species, including the aptly named Cleptocaccobius. Infestations can be high and brood survival can be significantly impaired; in one study 12% of Scarabaeus puncticollis nests were attacked by Aphodius brood parasites, and offspring rearing rates were reduced by 68%.

There are fly kleptoparasites too. Several species in the genus Ceroptera in Africa and Norrbomia in North America (lesser dung flies, family Sphaeroceridae) have only ever been reared from brood balls buried by dung beetles. The diminutive adults ride on the relatively huge roller or tunneller beetles, waiting for a chance to lay their eggs before the dung is finally interred.

Whether nest invasions are deliberate cuckoo infestations or merely casual visitors (or accidentally buried in the heave-ho scramble), the nesters know they must protect their brood supplies. If the roller detects that his or her dung ball has been compromised in the making, and has been invaded by endocoprids, it will abandon the task. In the mad flurry, at the height of the elephant dung beetle season, endocoprids can render a large pat useless to rollers in just 15 minutes. It’s a difficult trade-off, but despite the pressing urgency to get a dung ball to a safe distance, slower beetles may sacrifice getaway speed, but concentrate on creating a more solid, better consolidated, pest-free ball. They have to remain vigilant, though; females of the large European tunneller, Copris lunaris, will attack and kill Aphodius larvae if they find them in the nest.

Yes, killing, it crops up everywhere in nature, and is the keystone of every food-web imaginable. So whilst the dung flies and dung beetles are gently clearing away the mess, or even fighting roughly over it, there are plenty of predators attracted too. The hasty assault on a large elephant dropping has as much to do with avoiding being eaten by hornbills, guinea fowl and mongooses, as it does with getting a fair share of the pat. Not that a quick exit necessarily guarantees the safety of a beetle, or its progeny. Days or weeks after the work is done, buried dung beetle pupae are still dug up and eaten by ratels (also called honey badgers) and aardvarks. As was alluded to earlier, wasps and robber flies sit and wait on the dung for incoming prey, on which they pounce. And certainly dung flies, getting to grips with each other in mate-guarding and egg-laying bouts, are not above eating either each other, or the myriad other small flies hopping about. But there are also plenty of predation opportunities inside the dung too.

The rove beetles (Staphylinidae) are perhaps the most diverse beetle family on the planet, so it’s not surprising to find some of them live in dung. Though a few of the smaller slow-moving species (Oxytelus, and Anotylus species) are dung-feeders (as both larvae and adults), the vast majority found in the pat are predators. Some are very small, like the taxonomist’s nightmare genus Atheta, with who knows how many hundreds of species worldwide, none larger than 5 mm long. They, and their larvae, attack tiny invertebrates, especially young fly maggots. Then there are the larger, feistier species, including the large genera Quedius, and Philonthus, which can handle nearly full-grown maggots, and the handsomely mottled Ontholestes which dashes about at top speed around and under very fresh dung, snatching blow flies and greenbottle flies out of the air as they fly into the fresh dropping. These are quite spectacular to watch, and sure enough at my dung timing experiment near Reading one of the UK species, Ontholestes murinus, appeared in the first five minutes and had caught and made off with a hapless blowfly within moments.

Among the most characteristic of the predators are the oddly globose, shining and slow-moving clown beetles (family Histeridae). Quite how they got their common name is a mystery to me; according to some sources, Hister apparently means ‘actor’ in Latin (hence histrionics), and their flat legs, perfect for burrowing through the rancid mire, are reputedly likened to flat clown shoes and ill-fitting trousers. Seems highly unlikely. These chunky lumbering insects are never very large (12 mm maximum), but this belies their potency as ferocious predators of fly larvae. They are powerfully built, strongly armoured and have sharp protruding jaws. Their larvae, too, wade in on the attack. Dung is home to many species, but since their fly maggot prey will also breed in carrion, compost, rotten fungi and other decaying organic matter, histerids too are fairly catholic in their habitat requirements.

Not all fly maggots take on a passive victim status. There are also plenty of predatory grubs in the dung. Some, like those of the large bluebottle, Polietes lardarius, and the noon fly, Mesembrina meridiana, feed on dung material when they first hatch from the egg, but as they get larger they become more predatory, using the extra protein boost to finish their larvahoods, ready for pupation and the change to adults. Some larvae are predatory from the start, including a whole host of small nondescript grey and brown flies in the genera Helina and Hydrotaea. They may be diminutive, but there is always something smaller in there to get your teeth into.

Fig. 27 The chunky form of Aleochara is useful for burrowing into dung, but the adults are rather transient, laying eggs then departing.

A sadly understudied group of insects make up a poorly understood dark corner of the dung food-web – the parasitoids. These are mostly small or very small, slim wasp- or ant-like creatures in a broad range of families, including Braconidae, Ichneumonidae, Pteromalidae and Proctotrupidae; they are all in the same insect order (Hymenoptera) as bees, wasps and ants, but are only distantly related. Throughout all nature the parasitoids are highly numerous and massively important in the ecology of things, but such is their obscurity that there is no sufficient common name for them other than, collectively, parasitoid ‘wasps’. Unlike predators, which attack and eat from the outside, parasitoids start internally.

The usual process is for an adult parasitoid wasp to find an insect larva and lay its egg on or in it. The egg hatches and starts to eat its host, alive, from the inside. The host larva may continue living and feeding for some days or weeks, but its fate is sealed. It may even get to pupate and form a chrysalis, but only the adult parasitoid wasps will ever emerge, usually through a neat round hole chewed in the side of the empty husk of its host. At some point the host is overwhelmed by the alien developing within, and it dies. Incidentally, that is the difference between a parasite, which lives upon but does not kill its host, and a parasitoid, which does.

One of the problems with studying parasitoids is that the adults are usually found well away from their potential hosts, sitting in the herbage, resting on leaves or even visiting flowers. Sit and watch a dung pat for as long as you like and I’m prepared to wager you’ll never see one of them come near. It’s all very frustrating.

One genus we do know a little about are the scarab wasps of the genus Tiphia. These are much more wasp-like, closely related to the myriad species which make small tunnel nests in sandy soil and stock their brood cells with flies, beetles, spiders, bees or other small insects, on which their grubs will feed. Tiphia, instead of digging the hole first, then stocking it with larval food, goes off in search of a beetle grub that is already buried, and digs down through the soil to find it. You’ll still never see one on a cow pat though. It lays its egg on the grub or pupa and leaves its own maggot to get on with the gruesome demolition work, first sucking out haemolymph, then burrowing in and eating the viscera. Although Tiphia femorata and T. minuta parasitise Aphodius dung beetle larvae in Britain and Europe, they are also happy with non-dung-feeding relatives such as chafers (Rhizotrogus and Anisoplia species), which eat grass roots.

A large group of rather squat rove beetles in the genus Aleochara blur the boundary between parasitism and predation even further. The larvae are specialist attackers of fly pupae. They start gnawing on the outside, but then burrow in and complete their development inside the soon empty shell of the fly’s puparium (swollen chrysalis). When the adult beetles emerge they leave a rough jagged hole in the puparium skin, contrasting with the usually smaller and neater holes of true parasitoids.

We know so very little about the majority of parasitoids of dung-inhabiting insects, other than a few random specimens, almost accidentally reared from dung samples. It is mostly fly larvae that are infected, but no doubt, like Tiphia, there are parasitoids of beetle grubs too. This is a glaring omission. Elsewhere in insect ecology the importance of parasitoids is central to our understanding of how ecosystems work. They are as much a pressure on insect larvae as are predators higher up the food chain. Dung beetles are special, but entomologists really need to get to grips with the parasitic Hymenoptera if we are to bring dung study into the mainstream. Hmmm, maybe that’s just my wishful thinking.

¹ I’m also partly swayed by his note that the Hebrew words for beetle (we still use scarab and carab today) and cherub (k’rubh) could have easily been confused over centuries of oral then handwritten copying and recopying.