Call of Nature: The Secret Life of Dung

ON THE AFRICAN savannah, a pile of elephant dung weighing 20 kg may have an existence measured in hours; this is recycling at its most efficient. In the arctic tundra, reindeer droppings may remain untouched for 5,000 years (Galloway et al. 2012), and although they can be useful in informing us what prehistoric caribou ate, for the dung fauna they are just frozen nuggets of a promise unrealised. Somewhere in the middle is the time scale appropriate for a dung pat near you.

However, even at a single fixed locality, the life span of a pat will vary. Since it is a complex community of organisms doing the dung recycling and removal, the pat moves at their pace, and this will change with the season, the temperature, the climate and the weather. Standard decay times for a cow pat in the UK vary from 35 to more than 150 days. In California they sit around for 360–1,000 days. In New Zealand 520 days are quoted. In Canada the figure is ‘up to years’: I suspect the dung-watchers finally ran out of patience, or their funding stopped and they had to call it a day.

Season is all important here. After the success of my May beetle-luring experiment down near Reading, I revisited the site that September and thought I’d repeat the exercise. There were a few flies, but though I waited half an hour not one beetle put in an appearance. It seems the dung beetles of Padworth were spring species. Britain does have summer and autumn dung visitors. The noon fly Mesembrina is widely quoted as being on the wing from late April to October, but this is a July and August insect as far as I’m concerned. I especially associate it with my childhood holidays to the Isle of Wight, Purbeck and Lyme Regis, where grazing meadows abound, and I was in a mood to chase large black flies with my home-made insect net. August and September are top months for the slightly fuzzy dwelling beetles Aphodius obliteratus (which quickly obliterates a pat in the hot sun) and A. contaminatus (which I think is unfairly named). Late autumn is my time to look for the rare A. consputus, which I’ve only ever found in October (flood refuse near Alfriston 1974, and dog dung in Friston Forest 1975). It may be ‘rare’ because fair-weather entomologists have retreated into their studies for the damp months of late autumn. The minotaur beetle, Typhaeus typhoeus, is active all winter from October onwards, and is regularly found struggling with rabbit pellets, dragging them, rather than rolling them, to a deep burrow in the sandy soil, in January and February. This marks the start of the main nesting season for this lovely insect in northern Europe (Brussaard 1983). It is one of the first beetles to fly into the moth traps of lepidopterists, when they tentatively put a bright mercury vapour light out in March.

In temperate Europe our seasons are temperature regulated, but in the tropics the permanently warm year is driven by alternating bouts of wet and dry. Those fantastic reports of vast beetle numbers arriving at elephant pats are all for the wet season. This is when the beetles waiting in their subterranean pupal chambers are able to break out, pushing up through the moist soil, no longer dry and concrete hard, to find new pats. As the dry season arrives, the number of beetles attracted to dung steadily declines, until the amount they remove becomes negligible. Termites continue to remove a trickle of dung material (Freymann et al. 2008), but even they peter out. So rather than being gone in a matter of hours, a pile of elephant dung can easily remain for 4 months, and one monitored heap persisted for 850 days.

Fig. 36 The winter-active minotaur beetle, Typhaeus typhoeus.

Exact times are somewhat irrelevant, then, but there is a slightly predictable process from newly dropped faeces, to the point where you’d never know there was anything there in the first place.

Assuming the dung boluses are not removed in ultra-quick time by hordes of eager tunnellers and rollers, a dung pat’s maturation might go something like this:

This is my personal take, anyway, based on exhaustive researches at the dung face over the last 40 years. So this chapter now follows a nominal British or European cow pat or horse dropping from delivery to removal.

Most of the book so far has been about this stage: the first appearance of the dung and the first arrival of the creatures it attracts. It might last hours, it might last days. The waves of flies and early-arrival dung beetles get stuck in as quickly as they can. It’s a time of bustling activity. This is the opportunity to sit and watch fresh dung, as the flies skitter around on the surface and the beetles plump down in the grass, then push their way underneath.

Ironically, there may be an initial negative impact on the environment immediately around the dung, especially if urine is also released. This can scorch the ground. High nitrogen levels, from the urea, uric acid or ammonium compounds, are toxic to plants, and the surrounding vegetation can be seared. I was beginning to worry about the patches of browning grass on my uneven lawn, fearing they may be some alien fungal disease, but I later spotted one of the cats squatting over it. Little monster. It is the mix of uric acid in bird droppings that makes them relatively unpalatable to dung-feeding insects, and a reason to dismiss dinosaur dung beetle claims. The cats, though, defecate elsewhere, in the flower beds, so visiting dung beetles, often the attractive Onthophagus coenobita, are not too put off. Cows and horses also tend to release their different bodily wastes in separate motions, so dung released in the open space of the grazing meadow is unlikely to be polluted with urine.

This fresh stage may last a few days or a couple of weeks in sunny southern England and is, to my mind, the most productive and interesting phase. The dung maintains its softness, so is easily manipulated when turning it over or cutting it open. This is the stage where the dung fauna is made up mostly of adult beetles that have arrived to feed and breed, and every dropping might hold some new treasure hidden beneath it.

There is a tale, based in truth I’m sure, but clouded by the fact that several slightly different versions have been recounted to different listeners. My old friend Roger Dumbrell told of a beetling trip where he and A.N. Other (name withheld by request) went to Camber Sands, near Rye, in East Sussex, back in the early 1970s before I really knew him. Walking onto the dunes from the car park they passed a large dropping on the sand and paused to consider whether or not to examine it. It was obviously fresh and the used tissue close by gave no doubt that this was a human discharge. One of them walked on, unwilling to engage that particular taboo, but the other gingerly turned the dung over with a stick. The beetles underneath were the very rare Onthophagus nuchicornis, and as the cry went up the previously unwilling coleopterist shelved disgust and came back to join in the exploration. Who walked on, and who first dived in, is now lost in the debate fogs of hazy memory, but the specimens remain in the collection, dated 4 May 1972, recorded as being under dog dung. Mind you, this is the same Roger Dumbrell who refused to write ‘under an old shoe’ in his catalogue, when he found a rare ground beetle under flood refuse in a saltmarsh; instead he wrote ‘under rejectamenta’. There was a time when an entomologist would write ‘in stercore humano’ in a published article, hoping the use of a classical language would somehow excuse or disguise his questionable behaviour. Incidentally, the name Onthophagus derives from the Greek ονθος onthos ‘slime’, and φαγειν phagein ‘eating’, particularly apt for a group of beetles often found under the riper droppings of omnivores and carnivores.

Fig. 37 Onthophagus, a name meaning ‘slime-eater’ occurs in some of the riper, more fragrant dungs, including those of cat, dog and human.

Whatever the origin of the dung, the first few days are the time for colonisation. First come the dung-feeders, with numbers peaking around the second day. After about 3 days predator numbers increase, peaking about another week later. In a famous study of beetle succession in Finnish cow pats (Koskela and Hanski 1977), 10-day tallies showed there were more carnivores in the dung (average 191 individuals, of 16 species) than coprovores (126 individuals, 11 species); but the biomass (total weight of all the beetles together) was greater in the dung-feeders (443 mg) than the predators (129 mg). The later arrival of the predators makes evolutionary sense; if you are a carnivore, better to wait until there is a thriving bustle of colonists on the dung before launching in on the attack. The study did not measure numbers or biomass of fly maggots, but since most predatory dung beetles are maggot-eaters, it also makes sense to wait until at least the first generation of fly larvae are up and running.

After the initial influx of new colonists, by about the second week of lying in the field, the pat no longer attracts hordes of new visitors. It arrives at a sedentary phase, where the developing larvae and maggots feed quietly within. Adult beetles are still present, but there is also movement off to new pats. The outer layer starts to dry, but the interior remains moist. This is the stage at which dissection skills really count.

I now look back on my early dunging life and sometimes regret the carefree exploration of so many pats teeming with life. I was careful to look for new and unusual species, but found the great numbers of common fry a mere distraction. This was a time of community dunging, when I might be in the company of Messers Dumbrell and Hodge, my father, and possibly other budding entomologists. When three or more of us surrounded a heavy horse dropping on a cliff-top path near Brighton, on 14 September 1974, I was pleased to note two different colour forms of the scarce Aphodius scybalarius (now called A. foetidus), and the equally uncommon A. foetens. But I did not count the exact numbers of what must have been of the order of 200 specimens of several commoner species, or make any assessment of the multitudinous larvae squirming in the fibrous mass. Thankfully other more mindful entomologists have gone into the numbers. The Finnish cow pats of Koskela and Hanski (1977) yielded a total of 62,498 beetles, of 179 species, gathered from 312 carefully arranged 1.5 kg dung masses. Coincidentally that’s about 200 specimens per pat, so I’m relieved that my memory appears to serve me well.

This is the time of greatest invertebrate diversity in the well-mined dropping. Although less obvious in temperate Europe, subtropical pats soon start to show a skewed sex ratio of dung beetles; males dominate the upper pat as females become increasingly subterranean, buried with their dung brood balls.

The single entity extruded at the beginning of the process has developed subtle moisture and temperature gradients, and each dung insect chooses its own very particular niche. There are huge size differences, and even in a British pat, with our impoverished island fauna, the heaviest dung beetle (one of the dors) can be 5,200 times as heavy as the lightest feather-winged beetle (see below). Tiny insects dominate, and despite 200 Aphodius dung beetles seeming a lot to me, this is nothing compared to a recorded 20,000 owl midge larvae in a single dropping. This diversity does not last long, though.

The early arrival of fast-breeding flies and get-in-there-quick beetles reaches peak activity in the first fortnight, but tapers off quickly thereafter. By about 8 weeks, after being riddled with adult and larval activity, and following sequential wetting and drying in Europe’s notoriously changeable weather, the dung is starting to look more fibrous; the pat is no longer a cohesive whole, but it starting to fray around the edges. Cattle dung often starts to show a bloom of the small orange ascomycete fungus Cheilymenia fimicola. This is the beginning of the end.

By this point, the familiar dung odours have evaporated, the bacteria that made up so much of the dung have been eaten, or gone into quiescent spore mode, and the dung really does look just like mushed up hay or processed plant material. There may still be a few dung beetles hanging around, but this is at the tail end of their interest. This is now a time for fungus.

Most of the fungi feeding in dung are small (microscopic really) and poorly understood. There are mind-boggling numbers of them. One millilitre of sheep dung can contain a million fungal mycelia (each mycelium being the fungus equivalent of a root system), and a gram of cow dung can have two million yeast cells, yeast being single-celled fungi. Despite a common misconception, fungi are not plants, they are a separate group of organisms. The best way to consider fungi is think of them not as producers (like photosynthesizing plants) but, like animals, as consumers. However, unlike animals, which do their digesting on the gastrointestinal inside, fungi do their digestion on the outside, absorbing nutrients with their tendril, root-like hyphae.

Many of the fungal spores are already in the dung when it is delivered, having been resting on the plants eaten by the animal in the first place. They remain inert, passing unharmed through the herbivore’s digestive tract until they are voided and can get to work on the dropped dung. The fungi are encouraged by the burrowing of the beetles aerating the dung. Occasionally they will throw up a fruiting body to produce spores. Most of these fruiting bodies are also microscopic – moulds and mildews – but the odd toadstool sometimes appears. For those who are interested, there is a useful guide to British coprophilous fungi (Richardson and Watling 1997); the authors suggest incubating sample material on a table in a warm room, between sheets of absorbent paper, or perhaps maturing in a glass casserole dish or plastic sandwich box. In his book on British cup fungi, Dennis (1960) exhorts: ‘A rich harvest may well await the man who cares to devote his leisure hours or his declining years to a study of stale dog dung.’ And you thought entomologists were disgusting?

Dung lying in the fields also sprouts up fruiting bodies. These can be highly distinctive, such as the delicately sheened egghead mottlegill Panaeolus semiovatus, or the more robust dung roundhead Protostropharia semiglobata. My favourites are the ink-caps, several Coprinus species. These large, distinctive mushrooms, with tall, elegant, almost cylindrical domed hoods, get their English name from the black dripping inky deliquescent mess which they become after producing spores, but the scientific name is obviously from the Greek word for dung. We used to find these often, when out on family rambles, and my father would collect them for a tasty snack on toast later that evening. He could eat them with impunity, him being a teetotaller, and all. Be warned, though, if you ever have these succulent fungi with a glass of wine, you’ll feel pretty bad afterwards. They contain a compound called cyclopropylglutamine (sometimes also called coprine) which blocks the enzyme acetaldehyde dehydrogenase, part of the natural metabolism of alcohol in the human body. This leads to a build-up of acetaldehyde, one of the chemicals that makes ‘off’ wine smell unpleasant, and which is often blamed for producing hangovers. Symptoms of the resultant aldehyde poisoning include facial flushing, nausea, vomiting, palpitations and general malaise – exactly like a hangover.

Meanwhile, back in the dung, the presence of countless fungal bodies and spilled spores now attracts another host of insects, this time fungivores. To be honest, for many of the smaller insects, it is not actually very clear whether they and their larvae are feeding on the dung, microbes such as bacteria, or on the fungi. These are mostly very small fry indeed, microscopic feather-winged beetles (family Ptiliidae) half a millimetre long, ridged rove beetles (Micropeplus species), tiny globular mould-feeders such as Atomaria and Ootypus (family Cryptophagidae), and the tiny larvae of very many groups of fungus gnats (families Sciaridae, Mycetophilidae, etc.).

Outwardly, the dung is on its last legs, crumbling to pieces, becoming powder even. Plants are growing up through it, and it is very quickly being reabsorbed back into the landscape. It is soon very little different to the other general leaf litter, so it’s no surprise that general leaf-litter organisms start to invade. Here are multilegged millipedes and centipedes. The gnarled flat-backed millipedes, Polydesmus, are probably genuinely feeding on the dung, they also occur under rotten logs, chewing at the fungoid decay. The shining black snake millipedes, things like Tachypodoiulus, are general leaf-litter scavengers, but they regularly appear as the soil–dung boundary becomes less defined. The centipedes are predators, hunting after whatever small soil-dwellers they can get; these will be various soft-bodied soil-dwelling invertebrates such as springtails, and bristletails, but also any lingering fly larvae.

Fig. 38 Cylindrical snake millipede, shaped for borrowing in the rapidly blurring dung–soil horizon.

Before it finally gives up the ghost, the dung, now in pieces, can be home to just about any soil surface inhabitant. Woodlice may feed, but they are also there for shelter. Root-feeding insects such as click beetle larvae (wireworms) and crane fly larvae (leatherjackets) make little distinction between tough cellulose grass roots and the final fibrous cellulose chaff from the dung. Ground beetles (Carabidae), smooth, sleek shiny predatory species, push through the root thatch, and have specially muscular back legs for wedge-pushing into tight spaces; they end up hiding and hunting under dung, just as they would under a rock or a log.

Ants feature little in most books on dung ecology, but they are a regular feature of older horse droppings. Soil-nesting species may be attracted by moisture if the weather has been warm and dry for some time; predatory species may well be hunting after small prey items.

There comes a point at which the dung is no more than a memory. The grass grows a little greener, but there is no physical evidence that a pat ever lay on top of it. Forensic sifting of the soil might reveal a few fragments of insect remains, bits of beetle left over from predatory attacks or subterranean breeders unable, for one reason or another, to escape the final binds of their interment. These remains last a long time, and they continue to remind us what was in the dung, even millennia later.

One of the remarkable discoveries of palaeo-biogeography was the remains of 150 subfossil specimens, and bits of specimens, of a dung beetle from peaty deposits in a gravel pit at Dorchester on Thames near Oxford in 1973. They proved to be Aphodius holdereri, a dweller dung beetle now restricted to the Tibetan plateau, 3,000–5,000 m on the north side of the Himalayas (Coope 1973). This is about as high as dung beetles get anywhere on the globe. The Oxford deposits, together with a further 14 sites in England where this species later turned up, are dated to the middle of the last glaciation, 25,000–40,000 years ago. With a change in the climate, and the retreat of the ice, this particular cold-adapted dung beetle was not able to survive in Britain, where it was once obviously widespread (feeding in caribou droppings?), or anywhere else in the world, except the extreme centre of Asia, where it clings on in yak dung, or whatever it can find.

That beetles, at least, remain buried in the ground long after the dung has vanished is obvious to anyone who has ever seen the rains arrive in north Africa. It was here, 4,000–5,000 years ago that the marvel of the sacred scarab was first observed, or first revered. Though they have spent many months chewing away inside their dung balls, the scarab grubs have transformed into pupae and finished their development, but remain quiescent, waiting. They are, quite literally, entombed in a rock-hard nodule, and the dry ground above them is compacted and solid, sun-beaten and parched. They will only emerge when rainwater has softened the impacted clay, pushing up through the now blank and featureless soil, erupting through the surface of the ground, as if by spontaneous generation. But there was always the danger they might never escape.

At Poona, western India, in June 1826 Lieutenant-Colonel W.H. Sykes was having some of his palanquin-bearer servants dig and break up hard ground with pick-axes to spread on his garden paths, when they encountered ‘some depth below the surface, four hard perfect balls. At first they considered them stone cannon-shot.’ The Colonel, however, recognised that a broken ball contained the crushed remains of an insect pupa so he kept two of them in a tin box in his study, to see what would emerge. He soon forgot about them, but on 19 July 1827 he heard an eerie low scratching sound coming from the abandoned tin, now stuffed on top of a bookcase. He realised that some beast was trying to extricate itself from the hard clay ball, but by one o’clock in the morning it had not succeeded so he went to bed. It continued its ineffectual scratching all the next day too. Finally, before heading off to his bedroom, he doused the ball in water and at sunrise on the 21st he found a fine specimen of the glossy black Heliocopris midas. The other emerged on 4th October. They had been in his possession for 13 and 16 months, respectively, and he estimated that they had been underground for three years before they were dug up (Sykes 1835).

These ghosts of dung life past can still be located well after the dung, and the dung-droppers, have gone. Large fossilised dung balls, 20–50 million years old, are known from South America, even though the mammalian megafauna that provided the raw materials, are long extinct – huge armadillo-like creatures the size of small cars, giant sloths bigger than polar bears and bizarre elephantine hoofed creatures. No fossil beetles are known here, but their empty rolled and buried dung balls are distinctive enough for several Coprinisphaera species to be named in the scientific literature. Some of the dung balls are whole, suggesting that their inhabitants never emerged. Others show the belated chewings of other creatures, cuckoo parasites, enough for these also to be named; several Tombownichnus species were most likely kleptoparasitic beetles, and Lazaichnus fistulosus looks to have been a worm of some sort (Sánchez and Genise 2009).

Back in the modern world, other secret contents in the dung balls, whether rolled away or buried beneath, are the seeds which the original herbivore (or frugivore) swallowed, and which were passed in the primary dropping. Unbeknownst to the busy beetles, they have nearly finished assisting the plants that started the whole nutrition chain in the first place. Just like the Spanish dumbledor, Thorectes, which helpfully buries acorns well away from the overshadowing parent tree, so too the much smaller dung beetles have taken around 25% of the seeds in the dung and neatly buried them carefully a few centimetres deep in the rich fertile soil (Shepherd and Chapman 1998; Beaune et al. 2012). Here the seeds escaped the attentions of sparrows, harvester ants and spiny pocket mice and are perfectly placed to germinate in months or years to come, to found another stand of tasty plants for future grazers, and future dung providers. It’s a circle-of-life kind of thing.

Back at our nominal European cow pat, a year is as good a suggestion as any to declare that all outward signs of the original dung are gone. But the buried pupae of tunnellers and rollers are probably somewhere nearby. When we uncovered dor beetle pupae in the shallow soil of the Iron Age archaeological dig above Newhaven it took a few moments to realise what they were. Although many of the meadows round about were grazed, there were no animals where we were, nor were there any outward signs of their faecal signatures. Had we not disturbed them, the dumbledors would have clawed their way up through the soil a few weeks or months later, and made the short journey to the next field, where cows still chewed the cud, and where fresh pats were awaiting attention.

In moist, rain-drenched Britain it is easy to forget how rock-hard the soil can get when it really dries out, but the ancient Egyptians were right to be in awe of shiny black scarabs disgorging themselves out of the soil when the crop-giving rains returned in October. Whether they associated the beetles with a circle-of-life seasonality of crops and harvest, grass growth and grazing meadows, or the mystical daily cycle of the sun rolling through the heavens, it was something they wondered at, and applauded. What, then, would they have made of the modern-day decline of dung beetles? Could they, horror of horrors, contemplate a world where the dung beetle was no longer pivotal in the cycling and recycling of the world’s ordure?

fresh	hot on the ground, steaming, ready and waiting
mature mined	the first flush of incomers are breeding maximum occupancy of various life stages, overlapping generations
mouldy	initial attractiveness is wearing off, the pat is drying
mouldering	no longer a cohesive unit, weathering, fraying at the edges
crumbling	falling apart, pecked apart, disturbed by plant regrowth
ruins	just bits of dung, fragments, leftovers
dregs	powdery remains, a dusting of particles
echoes	no dung left, but there is evidence it was once there
ghosts gone.	the occasional reminder