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AT THE start of the 16th century, France and Spain were scrapping over
Naples like two dogs over a bone. Eventually, the Spanish army pinned down
the French in Uovo Castle, but the fortress was naturally well protected
and the siege seemed likely to drag on for months. Then, suddenly, on 26
June 1503, there was a massive explosion. The hero of the hour was Pedro
Navarro, a military engineer, who had successfully burrowed into the rock
beneath the castle, packed the tunnel with gunpowder and blown the fortress
to pieces. As Uovo suggests, and reflection will confirm, burrowing in all
its forms – sapping, mining, building the Channel Tunnel, or burying radioactive
waste – occupies a central place in human affairs.

Burrowing animals of other species cause less controversy, but their
ecological impact is no less important. Researchers now detect their influence
on matters ranging from plant diversity to movements of plutonium in the
Irish Sea. Many burrowers play vital roles in nature’s economy. Earthworms,
for example, work the soil more efficiently than any plough, aerating it,
fertilising it and improving the drainage in one smooth operation.

This underground activity is not confined to dry land. Intertidal mud
and sand are home to a worm every bit as industrious: the lugworm Arenicola
marina. Lugworms live head down in J-shaped burrows and make their living
by eating the sediment, extracting nutritious particles – bacteria and dead
organic matter – and passing the rest to the surface in the form of the
familiar wormcasts. This languid lifestyle seems simple and its effects
parochial, but appearances are deceptive. Lugworms are 20 centimetres long
(up to twice that size in offshore sediments) and they can live at any density
up to 150 in a square metre. As they burrow, they churn the mud and aerate
it, creating ideal conditions for bacterial decomposition. By eating the
mud and ejecting their faeces they mix it further. Lugworms are also accomplished
‘gardeners’; their casts sprout a burgeoning population of bacteria, which
can then provide a nutritious alternative to ordinary mud.

Lugworms, in turn, are food for a range of predators. In the Waddenzee,
off the Netherlands, half the food of young plaice takes the form of lugworm
tails. Because tips of tails regenerate quickly, the average worm can feed
a plaice many times each year without suffering any lasting injury, except
to its dignity. A patch of lugworms is, so to speak, an animal lawn and
the plaice a living mower. Dead bodies, bacteria, lugworms and carnivores
make up a macabre, but sustainable, strand in the overall economy of the
area.

The effects do not stop here. Lugworms and their compatriots radically
affect the physical properties of the sediments they occupy. According to
Peter Meadows, a marine biologist at the University of Glasgow, burrowing
animals increase the area of the interface between sediment and water by
a thousand times, opening broad highways for chemical traffic between the
two zones and creating extra living space for microbes. Vertical burrows
irrigate otherwise impermeable sediments and transform their chemistry.

What makes these effects so important is the densities at which burrowing
animals live. The crustacean Corophium volutator, which builds a U-shaped
tube about four centimetres deep, lives in flocks numbering 11 000 to the
square metre. Nereis diversicolor, a worm whose excavations can reach 40
centimetres beneath the surface, enjoys the company of up to 4000 companions
per square metre. When researchers use special quick-setting resin to make
casts of the burrow systems on the floors of estuaries, the result is a
staggeringly complex tangle of tubes. Because every tube has a mucous lining,
the sediment is made stronger and harder to erode. Lugworm casts are similarly
resistant to erosion because they are compacted and bound with mucus. Meadows
and his colleagues in Glasgow estimate the shear strength of a sediment
(a measure of its resistance to shearing forces, such as those exerted by
a water current overhead) by using a penetrometer. This device monitors
the depth to which a metal cone sinks into a sediment when falling under
its own weight. Shear strength can then be calculated by resort to a standard
equation.

The tests show that Corophium can treble the shear strength of its muddy
home if present in large enough numbers. Observations with a scanning electron
microscope confirm that the grains of such a strengthened sediment are bound
together by animal secretions. When such a sediment finally erodes, the
particles take much longer to settle than those from ordinary sediment,
for reasons that have yet to be established. Whatever the explanation, they
are likely to travel further before coming to rest.

Such effects are of direct relevance to human enterprises. Once a buried
oil pipeline is disinterred by erosion, it feels the full force of the sea
and is more easily fractured. Migration of sediment in harbours and estuaries
is an equally unwelcome consequence of erosion.

Research is only now beginning to unravel the ways in which burrowing
animals influence such events, yet no one doubts that they are important.
Eventually, it may be possible to harness their skills and prevent erosion
in critical sites – that is the eventual aim of Meadows and his colleagues.

On land too, burrowing creatures can influence the pace of erosion.
The Welsh island of Grassholm, for example, teemed with puffins until their
excavations destroyed the soil and deprived the birds of suitable nesting
sites. Yet the link may not be as simple as it appears at first sight, according
to Robert Furness of the University of Glasgow, who is following the fortunes
of burrowing birds on the Scottish isle of Rhum. His work suggests that
under some circumstances birds can stabilise the soil.

Rhum is home to 120 000 pairs of Manx shearwaters which dig their burrows
at sites up to 800 metres above sea level. It takes a couple of shearwaters
several years to excavate a satisfactory home, and Furness finds that they
prefer to begin work in an area already suffering a modest degree of erosion.
Once the birds are installed in their burrow, they deposit a hail of guano
on their front doorstep. Unwittingly, the birds encourage the growth of
a luxuriant flora, which binds the soil and slows erosion. Over a small
area, the scale of this deposition of fertiliser is enormous. On the Shetland
Island of Foula, for example, breeding puffins add 314 grams of nitrogen
a year to every square metre of soil they contaminate – a thousand times
as much as that arriving via rainfall.

Champion sand swallowers

Marine burrowers fertilise their surroundings in a similar fashion,
but they can also liberate nutrients in other, more important ways. One
is bioturbation – the general stirring that comes from digging and feeding.
This art is brought to perfection by the lugworm and its contemporaries.
The various species of animals eating a sediment can pass the top 10 centimetres
of their habitat through their bellies in less than five years. A Californian
worm by the name of Thoracophelia, which weighs in at 0.04 grams, eats 84
grams of sand a year – more than five times its own weight every day. (As
this example demonstrates, mud is not very nutritious.) Offshore, burrowing
shrimps, predatory worms and fish cause much disruption with their excavations,
which may descend 2 metres or more into the seabed. Bioturbation persists
even at great depth: burrows have been found 5 kilometres deep on the floor
of the Atlantic Ocean.

Marine sediment acts as a kind of recycling plant, in which bacteria
turn dead animals and plants back into simple chemicals, which can be exploited
again by other living organisms, such as marine algae. Burrowing animals
accelerate the entire process. In an unoccupied sediment, only the surface
layer is supplied with oxygen. As burrowing animals sink their shafts into
the black ooze beneath the surface, they bring oxygen-rich water to new
areas. This creates extra living space for oxygen-loving bacteria, which
thrive in the burrow walls and pursue their vocation of splitting organic
matter back into its chemical constituents. The burrowing crustacean Corophium
volutator increases the amount of oxygen-rich sediment in its neighbourhood
by 150 per cent.

At Odense University, in Denmark, Frede Andersen has measured the extent
to which burrowing animals stimulate bacterial activity. By monitoring the
rate of oxygen uptake in sediments both with and without burrowing animals,
he has discovered that animals accelerate the rate by as much as three times.
Only a small part of this increase is attributable to the animals themselves;
the rest signals a large increase in the productivity of the local microbes.
Burrowing animals also enhance decomposition by bacteria that live without
oxygen. Water currents, set going by the animals as they feed, move or respire,
bring raw materials close to the microbes and help to dissipate end products,
such as ammonia.

Just as burrowing sea-dwellers supply nitrogen to floating algae, burrowing
land animals turn over the soil and bring buried nutrients to the surface.
Pocket gophers, for example, have played an important part in the recovery
of the region around Mount St Helens in Washington State, bringing soil
and seeds to a barren surface blanketed in volcanic ash. Elsewhere, verdure
around animal burrows often owes its existence to nutritious soil thrown
on to spoil heaps by enthusiastic diggers. Badgers’ setts and rabbit warrens,
for example, attract a nitrogen-loving flora dominated by elder and nettles.
The trained eye can often locate a sett from this characteristic vegetation.
Ants have an equally profound effect on the vegetation. Lasius flavus, the
yellow meadow ant, for example, creates mounds of soil whose vegetation
differs markedly from that of the surrounding area.

On a grander scale are the heuweltjies, of the western Cape province
of South Africa. Heuweltjies are circular mounds some 30 metres across and
2 metres high. They occupy up to a quarter of the land surface where they
occur. Researchers have put forward scores of ideas over the years to explain
their presence. Barry Lovegrove, a zoologist at Marburg University, West
Germany, believes that they are the combined handiwork of generations of
burrowing termites and mole rats.

Whatever the precise cause, Lovegrove and his colleagues have found
that the mounds differ sharply from the surrounding land. Their soil is
far more fertile, it is finer, with fewer stones, it holds water more effectively,
it tends to be alkaline instead of acid and has a higher concentration of
nitrogen, magnesium and calcium – all of which could be the work of the
burrowing creatures involved in the mound’s construction. As a result, the
flowering plants growing on the mounds are far more diverse than those of
the surrounding country, often by as much as 30 to 40 per cent. Without
the mounds, the flora of the region would be distinctly impoverished – a
state of affairs that underlines the need to conserve them before they are
lost to agriculture.

Farmers have traditionally cultivated any heuweltjies that happen to
lie on their land. Because the soil is so fertile, the farmers probably
owe around 10 per cent of their harvest to their mounds, according to Lovegrove’s
calculations. Those rash enough to flatten them in the cause of easier ploughing
end up with less productive land. In the process they uncover a layer of
calcium carbonate beneath the surface, which then has to be removed at great
expense.

As the story of the heuweltjies shows, burrowing animals can have a
major impact on the topography of a region. On a smaller scale, structures
such as anthills and spoil heaps increase the area available for plants
to grow and add to the living space open to small animals. On the shore,
tube-dwelling worms create voluminous sandy reefs that conceal all manner
of nooks and crannies suitable for other forms of life.

The effects of burrowing animals are not always so benign. Rabbits can
be a golfer’s, or an archaeologist’s, nightmare. A badger’s sett, which
can consist of 360 metres of tunnels sprawling over 750 square metres, may
occasionally pose serious problems to farmers. Spoil heaps ruin the smooth
terrain, cattle break legs by falling down the holes and tractors capsize
as tunnel roofs give way. Badger tunnels undermine roads and railway embankments,
leaving enormous repair bills in their wake. Tradition has it that a mole
undermined the British monarchy in 1702, when one of its earthworks in Richmond
Park caused William III to be flung from his galloping horse. The fall fractured
the king’s collar bone and precipitated his death.

Burrowing animals also influence the fate of environmental pollutants.
In Idaho, in the US, burrowing deer mice and kangaroo rats have colonised
a radioactive waste dump and made themselves at home among the buried isotopes.
By burrowing, they disinter contaminated material and open new routes through
which water can enter the dump.

In the Irish Sea, burrowing animals have comprehensively defeated human
intentions for the disposal of radioactive discharges. Researchers once
thought that plutonium released from the nuclear reprocessing plant at Sellafield
would become permanently buried in the sediment. Yet although discharges
have been cut, the amount of plutonium inside the local crustaceans has
not declined in the expected fashion. Long-buried plutonium is apparently
issuing from the seabed and entering the water column – with obvious consequences
for the local food chain. Storms probably ought to take some of the blame
for this exhumation, as the depth of water in the area is no more than about
30 metres, but burrowing animals are now under suspicion too.

David Swift and his colleagues at the Fisheries Laboratory of the Ministry
of Agriculture, Fisheries and Food, in Lowestoft, have surveyed the sea
floor in the relevant area with a view to making a mathematical model of
the effects of burrowing animals. The chief players in the drama turn out
to be a shrimp called Callianassa subterranea and an echiuroid worm by the
name of Maxmulleria lankesteri. Both burrow within the mud and feed on its
hidden riches.

The shrimp belongs to a group whose tropical members dig holes as deep
as 6 metres. Off Sellafield, Callianassa constructs a more modest affair
descending to 1.5 metres – still a substantial excavation for an animal
about 5 centimetres long. Swift and his colleagues have documented Callianassa’s
activities in the laboratory and reckon that a medium-sized shrimp could
excavate around 2 grams of mud each day. With up to 50 animals to the square
metre, small individual efforts combine to cause serious disruption to the
sediment.

Maxmulleria is equally industrious. It lives tail down in a J-shaped
burrow, 20 to 30 centimetres deep, and it feeds on surface mud with the
help of its ‘spoon’, a kind of flexible proboscis. After digesting the film
of algae and bacteria on the mud, Maxmulleria ejects the rest in its faeces,
some at the surface, some at the bottom of its burrow. It can live at a
density of up to 25 per square metre, so, like Callianassa, it has the potential
to create a good deal of bioturbation. Exactly how it influences the migration
of plutonium must await a more detailed understanding of its habits – work
that is now under way at the Scottish Marine Biological Association’s laboratory
at Oban. The moral of the story is plain. The Earth’s surface, both seabed
and soil, bears a patina of burrowing creatures, whose activities are too
important to ignore. They both sustain us and undermine us. From Uovo castle
to the Irish Sea, nature’s burrowers are a force to be reckoned with.

* * *

So what’s in it for the diggers?

BURROWING animals are ecologically important because they help in the
great task of recycling organic matter. Without them, soils and sediments
would be considerably less fertile. Yet animals scarcely burrow for the
good of the planet: what’s in it for them?

Protection from predators is a major boon, especially for vulnerable
grubs, pups and chicks. Such considerations unite animals as diverse as
dung beetles, which install their larvae in underground chambers beneath
cowpats, and sand martins, which rear their chicks in tunnels up to a metre
long.

Another compelling reason for burrowing is the exploitation of underground
food sources, such as roots and tubers, not to mention other burrowing animals.
Moles capture worms and store them in an underground hoard; one such cache
was found to contain 1280 victims.

Burrowing also creates a haven from the vicissitudes of climate, in
which temperature and humidity remain fairly constant. Without some retreat
from the midday Sun, small rodents would find desert life intolerable. Lungfish
survive arid periods by sealing themselves in a muddy tomb until the rains
return.

These are the obvious reasons for burrowing, yet they are by no means
the only ones. A species of scrubfowl, which lives on some volcanic islands,
buries its eggs in hot soil and neatly sidesteps the work of incubation.
Solitary wasps of the genus Bembix dig to confuse their enemies. After sealing
their eggs in an underground chamber, they excavate decoy burrows, as if
designing an entomological version of dungeons and dragons.

Burrows play an important part in communications. The burrowing owl
hisses from its retreat so that predators will think it a rattlesnake. The
mole cricket creates a complex underground chamber which acts as megaphone
and broadcasts its song. Spoil heaps outside the burrows of a species of
ghost crab function as advertisements, deterring rivals and attracting females.

Animals also put burrows to good use in the quest for food. Leaf-cutter
ants and certain termites build underground chambers in which to cultivate
their fungal gardens. The sandfish lizard tracks its victims from underground,
swimming through the sand before emerging to deliver the coup de grace.
Trapdoor spiders and the larvae of the antlion play a more sedentary but
equally deadly burrowing game.

* * *

Archaeologists smell a rat

AT Creswell Crags, Nottinghamshire, rats are rotting in the cause of
science. The experiment will eventually reveal the extent to which a rotting
carcass in a cave disturbs the sediment beneath it – a matter of great importance
in archaeology and related disciplines.

Researchers can extract a good deal of information from the way in which
sediments are layered on the floors of caves. A sequence of pollen grains,
for example, may reveal the successive vegetation of past ages. Because
burrowing animals can scramble that precious information, their activities
are now attracting intense interest. The chief culprits are insects drawn
to decaying corpses.

Enter the rotting rat. Jem MacDonald and Chris Terrell-Nield of Nottingham
Polytechnic are employing the rodent’s services in an attempt to find out
more about the process. They began by sinking a number of Perspex tanks
into the floor of a suitable cave at various distances from the entrance.
Using sediment from the cave, they filled the tanks, marking the sediment
at 5-centimetre intervals with small polystyrene beads and pollen grains.
A dead rat provided the finishing touch.

The experiments are still in progress, but several important findings
have already emerged. In deeper caves, which insects rarely reach, fungi
are the chief decomposers. Far from disturbing the sediment, their meandering
filaments appear to stabilise it. Closer to the outside, blowflies and their
allies are dominant. Unlike the fungi, they do disrupt the sediment by their
activities, but only mildly.

Another frequent visitor here is Quedius mesomelinus, the common cave
beetle which preys on blowfly maggots. The beetle’s larvae are accomplished
burrowers which probably complete their metamorphosis in a chamber within
the sediment. Beneath a rotting rat, their activities are enough to move
much sediment.

Much greater disruption attends the excavations of the burying beetles,
such as those of the genus Necrophorus. Provided the carcass is relatively
fresh and near the cave’s exit, Necrophorus will literally bury it. Having
interred the corpse, the female tends her young in a side chamber leading
off the grave itself and feeds them on regurgitated carrion. Not surprisingly,
burying beetles wreak havoc on the surrounding sediments.

The findings imply that archaeologists must be fastidious in their choice
of sediments for analysis. Some of the caves at Creswell were once the dens
of wolves and hyenas and they must have witnessed a veritable deluge of
carrion. Over the years, other caves have tended to trap any animal unfortunate
enough to fall in unawares. Either way, the insects have enjoyed a banquet,
but at the expense of corrupting the neatly layered message in the sediment.

Stephen Young is a freelance science writer based in Wales. This article
is based on ‘The environmental impact of burrowing animals and animal burrows’,
a conference held at the Zoological Society of London, 3 to 4 May.