The New Naturalist Library

A SURVEY OF BRITISH NATURAL HISTORY

CAVES AND CAVE LIFE

Editors

Max Walters, ScD, VMH

Professor Richard West, ScD, FRS

David Streeter, FIBiol

Sarah A. Corbet

Derek Ratcliffe

The aim of this series is to interest the general reader in the wildlife of Britain by recapturing the enquiring spirit of the old naturalists. The editors believe that the natural pride of the British public in the native flora and fauna, to which must be added concern for their conservation, is best fostered by maintaining a high standard of accuracy combined with clarity of exposition in presenting the results of modern scientific research.

A cave spider Porhomma convexum stalks across the floor of GB Cave on Mendip. Above it, a fungus gnat Speolepta leptogaster hangs in a spreading fungal mycelium. (Philip Chapman)

Copyright

William Collins

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This eBook edition published by William Collins in 2018

© Philip Chapman Philip Chapman asserts his moral rights to be identified as the author of this work

A catalogue record for this book is available from the British Library.

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Source ISBN 9780007308545

Ebook Edition © JANUARY 2019 ISBN: 9780007403974

Version: 2019-01-09

Dedication

Dedicated to the memory of

Dr G.T. ‘Jeff’ Jefferson

a dear colleague and friend

Contents

Cover

Title Page

Copyright

Dedication

Editors’ Preface

1. The Fascination of Caves

The lure of caves

The sporting science

Underground naturalists

2. The Cave Habitat

What is a cave?

What lives in caves?

Caves in Limestone

Types of cave habitat

Food supply

Microclimate

3. Limestone Caves in Britain and Ireland

Karst: the landscape of caves

Caves in Britain and Ireland

Mendip

Pennines

South Wales

Derbyshire’s Peak District

Sligo-Fermanagh

Clare

Other areas

4. Cave Fauna and Flora

The origin and classification of cavernicoles

Life on the threshold

A place of shelter

Waifs and strays

Denizens of darkness

Submariners

5. Cave Communities

The wall association

Terrestrial mud bank community

‘Batellites’

Pool surface associations

Freshwater stream communities

6. Caves Through the Pleistocene

The age of ice

Pleistocene survivors and recent colonists

Troglodytes

7. The Future of Caves

Cave conservation and the caver

External threats to caves, groundwater pollution and public safety

Impact of human activity on cave faunas

Conservation of cave-roosting bats

Limestone quarrying

Acid rain, caves and flue gas desulphurization

Cave SSSIs

Databases

Glossary

Bibliography

Index

Acknowledgements

About the Publisher

Editors’ Preface

To man, caves are the original shelters, sought since Palaeolithic times hundreds of thousands of years ago. To the adventurous amongst us, they are challenges to be explored, dark passages leading to unknown underground palaces and waterways, sometimes of amazing beauty. To the naturalists amongst us, they arouse our interest by their curious and unique life-forms, selected by the restrictive environments, and by their presence in areas of limestone country of outstanding beauty. Yet, as with other life, the plant and animal communities of caves form a cohesive and interacting collection of organisms, from bacteria to mammals, from lower to higher plants, depending on the varied local environments within the cave systems.

Here, then, is an ideal subject for the New Naturalist, taking into account not only the living natural history of caves, but also their origin, habitat characteristics, and what they tell us of past times. Indeed, as well as their living content of caves, the sediments within them are often the graveyard of past denizens of caves, such as the hyaena, as well as the prey of cave carnivores; and, of course, these sediments reveal past habitation by man through the present of bones and tools. So we have a fourth dimension of time to add to the natural history of caves.

It may be thought that cave communities would be one of the few remaining natural ecosystems surviving in the British Isles, protected by difficulty of access. As with other living communities more apparent and better known to us, this is not the case; they are perhaps more fragile than above ground communities, more easily disturbed and affected by man’s activities. To the natural historian the subject of caves demands a broad multidisciplinary approach. Dr Chapman has extensive experience of the many aspects of cave natural history. He has been able to integrate this variety, dealing with the essential geological and geomorphological background, the historical theme, and the natural history of caves, so presenting the naturalist with an outstanding and cohesive account of a unique and extraordinary ecosystem of wide interest.

1

The Fascination of Caves

The lure of caves

There is a curious fascination about caves that seems to affect people of all ages and all cultures. Even as children, we have a kind of longing for caves, seeing them perhaps as a place of safety, but equally as a source of adventure and excitement – a gateway to the unknown.

Our remote ancestors used the entrances of caves as habitations, but reserved their depths as hiding places for their most precious and powerful secrets – the painted, magical symbols which would ensure a continuing supply of game for hunting, and the earthly remains of their dead. Religion was born in caves, and even now the buildings of our Christian cultures retain atavisms of those earlier forms of worship; under the central part of the church lies the crypt, secret and dark – originally the burial place of saints and martyrs. It is perhaps also significant that the Mother of God should have appeared to Bernadette in a grotto at Lourdes, and should have consecrated the cave spring which welled up from underground.

In Japanese mythology the sun-goddess Amaterasu retreated at night to a cave, plunging the world into darkness. The ancient Greeks too gave prominence to caves in their mythology. Zeus, chief of Gods, was born in a cave, and of course the Greek hell lay below ground, and at its gates Charon the ferryman waited in his boat to row the souls of the departed across the black waters of the River Styx into a land of grief and eternal pain. In our own mythology, King Arthur, his knights and hounds are said to slumber still beneath a Welsh mountain, eternally awaiting the call to battle. Even today in parts of New Guinea, tribesmen will say that their ancestors were born directly from the earth through the womb-like opening of a cave.

With such a long cultural association between the darkness of caves, their chill and smell of decay, and the nameless terrors of the grave, it is not surprising that our ancestors should have equated caves with what they knew of volcanic vents and imagined the fires of hell in their depths. Dante’s Inferno is just one manifestation of an older oral tradition in Europe which told of animals, usually a dog or a goose, entering a cave to emerge days later from another miles away, devoid of fur or feathers and showing signs of singeing by infernal flames.

Lurid accounts of real caves are frequent in ancient literature. The Roman philosopher Seneca reported that a party of Greek silver prospectors who ventured underground had encountered:

“huge rushing rivers, vast still lakes, and spectacles fit to make them shake with horror. The land hung above their heads and the winds whistled hollowly in the shadows. In the depths, the frightful rivers led nowhere into the perpetual and alien night.”

Seneca adds that after their return to the surface, the miners “lived in fear for having tempted the fires of Hell.”

Fig. 1.1 Manner of crossing the first river in Peak Cavern, engraved by Cruikshank in 1797, from G.M. Woodward’s Eccentric excursions … in different parts of England & South Wales, pub. Allen & Co., London, 1801. (Courtesy of Trevor Shaw)

Perhaps the oldest written reference to a cave appears in a book about mountains written before 221 B.C. in China – a country where caves have been systematically explored and exploited over many centuries as water supplies and as sources of nitrates for fertilizer and for making gunpowder. The earliest surviving reference to a cave in Britain dates from around 200 A.D. in the writings of Titus Flavius Clemens, known as Clement of Alexandria. He writes:

“Such as have composed histories concerning the Britannic islands tell of a cavern beneath a mountain, and at the summit of it a cleft, and of how from the wind rushing into this cavern and reverberating from its hollows, an echo as of many cymbals is heard.”

Which cave this refers to is uncertain, but a location in either the Mendip Hills or Derbyshire would seem most likely since both areas were well-known as important centres of lead mining during this period. Current opinion favours the Great Cave of Wookey Hole which would undoubtedly have been known in Roman Britain and where, according to Balch (1929), a noise like the clash of cymbals can occasionally be heard.

Irish caves were also documented from the earliest times. The Annals of the Four Masters, written in 928 A.D., record the massacre of 1000 people in Dunmore Cave in County Kilkenny and if the abundant remains excavated there are anything to go by, the account may well be true.

The myth of the ‘howling cave’ resurfaces with Henry of Huntingdon in his mediaeval Historia Anglorum, written in Latin around 1135. He gives pride of place among the four “wonders of England” to a cave “from which the winds issue with great violence”. This one appears to have been situated in the Peak District and may have been Peak Cavern, since some time later Gervase of Tilbury, writing about this cave around 1211, states that strong winds sometimes blow out of it. The third of Huntingdon’s four wonders was also a cave, this time one situated at:

“Chederole where there is a cavity under the earth which many have often entered and where, although they have traversed great expanses of earth and rivers, they could never come to the end.”

This poses modern scholars with an interesting puzzle, for although there is indeed a well-known cave at Cheddar (open to the public as ‘Gough’s Cave’), it is short, easily explored and does not connect with the underground river known to flow beneath it. However, in 1985, cave divers Rob Harper and Richard Stevenson squeezed down a narrow pit in a forgotten corner of Gough’s Cave and emerged underwater into the main river, which they followed upstream to reach a large dry cavern, dubbed the Bishop’s Palace. The flooded system lies close to the water table, and the divers surmise that before the Cheddar rising was enclosed by a dam, the water level may have been low enough to permit entry into the now-flooded cave. On the other hand, the village of Cheddar (once known as ‘Cheddrehola’) is only some ten kilometres away from Wookey Hole, and Huntingdon may well have confused the two localities.

The surprising thing is not the doubts about the accuracy of Henry of Huntingdon’s accounts, but that he should have chosen caves for two of his four ‘wonders of England’. Other mediaeval chroniclers also mention caves and mostly follow Huntingdon’s accounts closely, as also do the various manuscript ‘Wonders of Britain’ or ‘Mirabilia’ which appeared between the 13th and 15th centuries.

In the 16th and early 17th centuries writers such as Leland, Camden, Drayton and Leigh, gripped by the Elizabethan romantic passion for ‘discovering the countryside’, penned lurid accounts of the caves they visited and of the legends and folklore attached to them. One looked forward to a planned visit to Wookey Hole with not a little trepidation:

“though we entered in frolicksome and merry, yet we might return out of it Sad and Pensive, and never more be seen to Laugh whilst we lived in the world.”

The early 17th century saw the rise of a craze for so-called ‘rogue books’ – sensationalized accounts of swashbuckling anti-heroes such as highwaymen and pirates, and some of these make reference to dastardly goings-on in the caves of Derbyshire. Sam Ridd’s The Art of Juggling (1612) portrayed Peak Cavern as a notorious centre of knavery, and Ben Jonson makes several allusions to this cave (under a different name) and its association with beggars and vagabonds in The Devil is an Ass (1616) and The Gipsies Metamorphosed (1621).

Later in the 17th century the Peak District and its caves continued to attract attention through the writings of Charles Cotton, best known for his collaboration with Izaak Walton on later editions of The Compleat Angler. Cotton’s fondness for caves may be not altogether unconnected with his habit of using them as a sanctuary when hiding from his creditors.

Fig. 1.2 An imaginary ‘straightened out’ view of Peak cavern. In the foreground are the rope-makers’ cottages. From a copper engraving titled The Devil’s Arse, near Castleton, in Derbyshire which appeared in Charles Leigh The natural history of Lancashire, Cheshire and the Peak in Derbyshire, pub. Oxford, 1700. (Courtesy of Trevor Shaw)

Daniel Defoe, the great traveller and polemicist, seems to have completely failed to appreciate the ‘Wonders of the Peak’ which so enthused his contemporaries. Dubbing them the ‘wonderless wonders’, he selects Peak Cavern for a particularly scornful treatment:

“… where we come to the so famed Wonder call’d, saving our good Manners, The Devil’s A--e in the Peak; Now not withstanding the grossness of the Name given it, and that there is nothing of similitude or coherence either in Form and Figure, or any other thing between the thing signified and the thing signifying; yet we must search narrowly for any thing in it to make a Wonder, or even any thing so strange, or odd, or vulgar, as the Name would seem to import.”

This seems a bit harsh, as the entrance to Peak Cavern is, I would have thought, impressive by any standards. On the other hand, Defoe goes right over the top in his reaction to nearby Eldon Hole: “this pothole is about a mile deep … and … goes directly down perpendicular into the Earth, and perhaps to the Center”. It is actually 75 m deep.

Although Defoe’s Tour was not intended to be a guide book, a series of revisions by various editors up to 1778 made it ever more like one; even going to the lengths of adding in descriptions of caves not included in the original version. The success of the Tour and the rise of the ‘picturesque’ movement in art and architecture (epitomized by the romantic landscape designs of Humphrey Repton) no doubt encouraged the early 19th century vogue of ‘curious travellers’ who sought out and explored previously neglected corners of the countryside in order to write about their experience. Where previously the ideal landscape had been one which showed the civilizing hand of man in formal gardens and straight avenues of trees, ‘wild nature’ now became fashionable. Any accessible landscape featuring dramatic cliffs and wooded gorges, crumbling ruins and, of course, caves, became a tourist attraction. A swelling tide of visitors headed for the fashionable delights of the Peak and Wookey Hole, the scars and potholes of the Yorkshire Dales, the seacaves of Scotland and Kent’s Cavern at Torquay. Even the great Dr Samuel Johnson seems to have been caught up with enthusiasm for a sea cave he visited on Skye during his tour of the Hebrides in 1773.

The descriptions by the ‘curious travellers’ generally aimed to convey emotions of awe, wonder or terror at the beauty and power of ‘wild nature’. Caves lent themselves particularly well to the Gothic imaginations of young romantic writers like Benjamin Malkin, who described a visit to the entrance of Porthyr-Ogof in his The Scenery, Antiquities, and Biography of South Wales (1807):

Fig. 1.3 Fingal’s Cave from a hand-coloured wood engraving by Whimper, in Anon: Natural Phenomena, pub. London, SPCK, 1849. (Courtesy of Trevor Shaw)

“We penetrated about an hundred yards, as far as any glimmering of daylight from the mouth directed us: and this specimen of Stygian horror was amply sufficient to satisfy all rational curiosity. The passage over uneven rocks, with scarcely a guiding light, and in many places with a bottomless gulph directly under on the left, in a misty atmosphere from the vapour of the place and the exhaustion of a laborious walk, was not to be pleasurably continued for any length of time or distance. … Any person who will enter this cavern … may form a just idea … of the classical Avernus and poetical descent into the infernal regions.”

The north-country clergyman John Hutton stands out among the ‘curious travellers’ as someone who developed a genuine interest in caves. His A Tour to the Caves in the environs of Ingleborough and Settle (in various editions from 1780 onwards) contained descriptions of some two dozen caves and potholes and was the first book in Britain, and one of the first in the world, whose main purpose was to describe the natural history of caves. In spite of his liberal use of Gothic adjectives such as “horrid”, “dreadful” and “terrible”, a real enthusiasm for his subject comes through, and in the two later editions of his book he added a section entitled “conclusions of a philosophic nature”, in which he discusses limestone geology, cavern formation and hydrology. Some of his views, particularly those on the springs and underground streams of the area, were farsighted, although others seem laughably quaint in the light of modern science. It is interesting for the modern reader to note the touchstone against which he measured his own ideas:

“I think I may say without presumption, that my theory is conformable to events as related by Moses; and my reasoning agreeable to the philosophical principles of Sir Isaac Newton, where they could be introduced.”

The early 19th century boom in natural science, when it spread to caves, focussed initially on two fields of research which Hutton had completely overlooked – namely palaeontology and archaeology. Deposits of bones had been known from caves in mainland Europe at least as far back as the 16th century, when speculation about their nature had inclined, as might be expected, to the fantastic. Some were considered to be dragon bones, while others – the sub-fossil tusks of elephants or mammoths, known as ‘unicorn horn’ – were greatly prized for their reputed medicinal properties. Quite an industry sprang up around such deposits, and their discoverers or the owners of the caves could become rich on the proceeds.

The Victorian naturalists were the first to appreciate the antiquity of cave bone deposits and their value as a geological record of Britain’s past. The best known of the early cave excavators was Dean Buckland, who plundered cave deposits throughout the country in the 1820s. In the interpretation of his results he was limited by the thinking of his day, but he recognized that many of the bones were from animals no longer present in Britain, and in some cases from animals that no longer existed at all. He was the first to suggest that the explanation for the accumulation of fossil bones in some caves might be that in the distant past hyaenas had used the caves as dens and dragged the carcasses of animals into them. Buckland also made the first find of an Old Stone Age human burial, the ‘Red Lady of Paviland’ found in Goat Hole on the Gower coast, so-called because her body had been anointed with ochre before burial.

Fig. 1.4 Gough’s Cave digging in early 1935, first published in Bristol Evening World, 1 Feb 1935. (Trevor Shaw collection, courtesy of Cheddar Caves Ltd.)

In the 1830s, Schmerling recognized that the remains of humans and of extinct mammals found together in the same deposits in Belgium were of the same age. It was not, however, until later in the century, that the work of William Pengelly and Boyd Dawkins and their colleagues established that these remains dated back thousands of years to the Ice Ages of the Pleistocene era, when cave-dwelling people shared our familiar countryside with a fearsome array of giant animals, including cave bears, hyaenas, woolly mammoth, bison, aurochs and woolly rhinoceros. Excavation in caves has, of course, continued to the present day, and cave sites worldwide have now yielded material which has helped to shape our understanding of human evolution and the birth of our culture.

The sporting science

The systematic exploration, documentation and commercial exploitation of caves was already underway in China many centuries before miners and natural historians first began to measure and record details of our European cave systems in a scientific way. One of the first of this breed of explorers in Britain was John Beaumont, a 17th century Somerset surgeon and an amateur student of mining and geology. When in 1674 lead miners excavating a shaft in the Mendip Hills accidentally breached a natural underground chamber, Beaumont hastened to the site and hired six miners to accompany him into the cave. Carrying candles, the company descended the 18 m shaft to the first chamber, which Beaumont proceeded to measure: it was 73 m long, two metres wide and nine metres high. “The floor of it is full of loose rocks,” wrote Beaumont in his subsequent report to the Royal Society, “its roof is firmly vaulted with limestone rocks, having flowers of all colours hanging from them which present a most beautiful object to the eye.” The intrepid surgeon then led a 100 m crawl through a further low passage which opened into the side of a second chamber, so vast, Beaumont reported, that “by the light of our candles we could not fully discern the roof, floor, nor sides of it.” The miners, accustomed as they were to the underground, could not be persuaded to enter this chasm, even for double pay. So Beaumont went down himself:

Fig. 1.5 Interior Chamber of Cox’s Stalactite Cavern, Cheddar, Somersetshire. Lithograph by Newman & Co. London; pub. S. Cox, Cheddar about 1850. (Courtesy of Trevor Shaw)

“I fastened a cord about me, and ordered them to let me down gently. But being down about two fathom I found the rocks to bear away, so that I could touch nothing to guide myself by, and the rope began to turn round very fast, whereupon I ordered the miners to let me down as quick as they could.”

He landed dizzy but safe 21 m below, on the floor of a cavern 35 m in diameter and nearly 37 m high within which he found large veins of lead ore. Surprisingly, Beaumont’s account failed to stimulate much curiosity about caves in scientific circles, and after a brief flurry of lead mining, the cave, known as Lamb Leer, was abandoned; its entrance shaft eventually collapsed and the sealed-off chamber was virtually forgotten for two centuries.

The rediscovery of Beaumont’s long-lost Lamb Leer cave took place in 1879, the same year that a young French law student, Edouard-Alfred Martel, made his first visit to the famous Adelsberg Cave in Slovenia (which was then part of Austria, but since World War II has reverted to its local name of Postojna Jama). Martel was completely enthralled, and in 1883 began to devote all his vacation time to cave explorations in the Causses of southwestern France. What set him apart from previous cave explorers, was his meticulous preparations and his systematic recording of all aspects of the caves he explored, combined with a tremendous physical ability and courage. His speciality was deep vertical pits, and in 1889 he successfully negotiated the 213 m vertical entrance shaft of the Rabanel pothole north-west of Marseilles – an outstanding feat given the equipment then available.

To calculate a pit’s depth, he would read the barometric pressure at the bottom and compare it with the surface pressure. He measured the horizontal dimensions of each newly-discovered chamber with a metal tape, drawing a sketch of the cave as he worked. Roof heights were calculated with an ingenious contraption: after attaching a silk thread to a small paper balloon, he would suspend an alcohol-soaked sponge beneath it, light the sponge, and measure off the length of thread carried aloft by the miniature hot-air balloon. Martel also habitually recorded subterranean air and water temperatures, finding variations with depth and season, and amassed whole volumes about cave geology, hydrology, meteorology and flora and fauna. But perhaps his greatest contribution to cave science was his research on how subterranean water circulates – a study prompted by his own bout with ptomaine poisoning, contracted from drinking spring water in 1891. After recovering from the illness, he traced the spring’s source using fluorescein dye introduced to nearby sink holes. Descending the appropriate pit, he found the putrefying carcass of a dead calf that had contaminated the spring with what he wryly termed “veal bouillon”. Further study allowed him to distinguish between “true springs”, fed by diffuse circulation of rainwater, cleaned and filtered by its passage through soil and rocks, and “false springs” fed by a rapid flow from sinkholes via cave passages too large to filter out impurities. Martel’s subsequent campaigning for stricter control of sources of drinking water eventually led to a dramatic reduction in deaths from typhoid and won him a gold medal from the French Government.

In 1895 Martel founded the French ‘Société de Spéléologie’, arguing that ‘speleology’, which had been previously considered a sport or a singular eccentricity, should be recognized as a fully-fledged science – “a subdivision of physical geography, like limnology for lakes and oceanography for seas.” A prolific author, he edited Spelunca, his Society’s bulletin, and wrote books about his own cave discoveries. In 1907 the French Academy of Sciences awarded him the grand prize for physical sciences, and in 1928 he was elected president of the Geographical Society of Paris. By the time he died in 1938, aged 78, the grand old man of speleology had personally probed nearly 1500 caves, hundreds of which had never been entered before; his technical innovations had become standard equipment for other cavers; and above all, his persistence and dedication had created a framework within which the seedling science of speleology could develop and blossom.

Meanwhile, the systematic documentation of caves had also started in Britain, with the formation of the Yorkshire Ramblers’ Club in 1892. Under the influence of S.W. Cuttriss, dubbed ‘the scientist’ for his assiduity in recording the group’s findings, its members drew up surveys of the caves they explored, and kept notes of temperatures, altitudes and geographical features.

The great exploration challenge of the day was the awesome Gaping Gill, a pothole high on the slopes of Ingleborough Hill which had been plumbed to a depth of 110 m, but had never been descended. The main obstacle to its exploration came from Fell Beck, an icy stream which cascades down the entrance, filling it with spray and extinguishing any flame which might light a caver’s descent, as well as half-drowning him. A local man, John Birkbeck, had made two heroic, but unsuccessful attempts to descend the pit in the 1840s, after digging a trench to divert the Fell Beck to another sink. His first try nearly proved fatal, when strands of his rope were severed on a rock ledge, but on his second attempt he reached a ledge at 58 m which now bears his name. Yorkshire Ramblers’ member Edward Calvert took up the challenge and had almost completed his own preparations for a descent on rope ladders in 1895, when Martel arrived on the scene, hot-foot from London where he had been invited to address an International Geographical Congress on cave-hunting methods.

As something of a celebrity, Martel was encouraged by the lord of Ingleborough Manor to have a crack at the great pothole and given the support needed to refurbish and extend Birkbeck’s trench. On August 1, before an eager crowd, Martel knotted together his lengths of ladder and lowered them into the darkness. As he climbed down the four metre-wide shaft he was rapidly enveloped by “half-suffocating whirls of air and water” which soaked his clothes and the field telephone which he relied upon to communicate instructions to the back-up team who controlled his safety line from the surface. The cascade redoubled 40 m down and he had to descend through a “frigid torrent gushing from a large fissure”. Pausing on Birkbeck’s ledge to untangle the huge heap of rope which had lodged there, he continued into the unknown depths below. Sixteen metres on, the walls of the shaft suddenly receded and Martel found himself swinging like a pendulum near the roof of an immense chamber nearly 160 m long by 30 m high. He alighted on the floor only 23 minutes after he began the descent, and characteristically at once set about measuring and sketching his discovery. For an hour and a quarter, the Frenchman revelled in the spectacle of the “Hall of the Winds”, Britain’s largest underground chamber from whose roof the waters of the Fell Beck tumbled “in a great nimbus of vapour and light”. There was a certain sense of nationalist triumph too: “The most pleasant feature was the thought that I had succeeded where the English had failed, and on their own ground.”

Fig. 1.6 Gaping Gill – the main chamber showing the waterfall falling 110 metres from the surface. A photograph taken in the 1930s by Eli Simpson. (Trevor Shaw collection)

Martel’s descent of Gaping Gill received wide publicity and awakened an interest in the possibilities of cave exploration in other parts of Britain. A group of Derbyshire rock climbers calling themselves the Kyndwr Club started to explore the caves of that county and further afield. One of their leading spirits was Dr E.A. Baker, a native of Somerset, but at that time resident in the Midlands. He was a colourful and influential character, an academic who later became director of the School of Librarianship in the University of London, but whose interest in caving was primarily sporting.

At about this time, H.E. Balch, a young postal worker at Wells in Somerset, came across a fragment of reindeer antler in the Hyena Den near Wookey Hole and, inspired by the work of Professor (later Sir William) Boyd Dawkins, at once threw himself into a study of all kinds of archaeological and fossil cave sites on Mendip. Soon Balch had founded the Wells Natural History and Archaeological Society and started the collections which eventually grew into Wells Museum. The subsequent arrival on the Mendip scene in 1902 of Baker and his colleagues from Derbyshire led to a long and fruitful collaboration, during which many of Mendip’s greatest caves were dug open and explored. Both Balch and Baker were prolific writers and their publications, spread over several decades, played a large part in stimulating an interest in caving during the early part of this century. A number of clubs began to appear which cheerfully combined a scientific and sporting approach to caving, setting a pattern which has continued to the present day. Scientifically motivated ‘speleologists’ still recognize their dependence on sporting cavers for much of the initial exploration and often for support when working in the more exacting situations. Many are in any case themselves sporting cavers, or were in their younger days. On the other side very few of those whose motives are primarily sporting are completely uninterested in the whys and wherefores of the natural features which provide them with their sport. They also appreciate that scientific understanding increases the chances of finding more caves.

There are few completely unexplored places anywhere on the surface of the earth and none in a country such as Britain; but caves hold out the promise, or at least the hope, of completely new discovery. Most cavers must sometimes dream of one day discovering a new cave, or an extension to a known one, and of being the first to gaze upon whatever wonders it may hold. If these are the things which provide motivation for caving as a sport, they are nearly always reinforced by at least some measure of scientific curiosity, and most cavers combine the two in varying proportions.

In the years after World War II, the popularity of caving, as of so many other active pursuits, increased enormously in many parts of the world. In Britain the 1950s and 60s in particular saw a great proliferation of caving clubs and, although some of these were ephemeral, the overall level of interest and activity has remained high. Perhaps the most important development in British caving in the early post-war years was the opening up of South Wales as a major caving region. Up until 1936, cavers had taken surprisingly little interest in the area considering that Porth-yr-Ogof had been known for hundreds of years and Dan-yr-Ogof had been discovered and explored as far as the waterfalls in 1912. It was to these two caves that experienced cavers from Yorkshire and Mendip first turned their attention in 1936 and interest in the area developed rapidly. By the time that caving came to a virtual halt with the outbreak of war in 1939, the potential of South Wales was apparent to all. In 1946 the South Wales Caving Club was formed and within a few months two of its members, Peter Harvey and Ian Nixon, dug their way into the lower end of the great Ogof Ffynnon Ddu cave system on the east side of the Upper Tawe Valley. Initially rapid exploration was halted by a series of sumps (flooded sections of passage) and it was not until 1966 that a dig in the upper levels of the cave gave access into the vast maze of OFD II. A rush of new discoveries followed in quick succession over the next year, extending the vertical range of the cave to 300 m and its total length to around 40 km, making it Britain’s deepest and longest cave system. (Although cave divers have since linked up various parts of the Ease Gill system in Yorkshire to give it the number one position with an overall passage length of over 70 km).

As we have seen, cave science, and in particular the archaeological and palaeontological investigation of caves, started well before the development of caving as a sport. As early as the mid-nineteenth century the living faunas of caves were receiving fairly extensive study in mainland Europe and America by the likes of J.C. Schiodte and A.S. Packard; and following the influence of Martel, the physical aspects of speleology – geology, geomorphology and hydrology – were well established there by the turn of the century.

Underground naturalists

Evidence that early man was conscious of the existence of a subterranean fauna dates back to a remarkable engraving of a cave cricket on a bison bone discovered by Count Begouen while excavating in the Grotte des Trois Frères in the French Pyrenees. The carving is believed to be 18,000 years old, yet is sufficiently clear and detailed for the subject to be recognizeable as a Troglophilus species, which today is distributed from Italy to Asia Minor, but no longer inhabits France.

For the next surviving reference to cave life in Europe, we must move on to the 16th century and the observant Count Trissino, who, in a letter dated 5th March 1537, recorded what must have been a form of the cave-limited amphipod, Niphargus. He noted that at the far end of the Covolo di Costozza in northern Italy there was a deep pool of clear water. “In this water no fish of any kind are found, except for some tiny shrimp-like creatures similar to the marine shrimps that are sold in Venice.”

Fig. 1.7 A prehistoric engraving on a bison bone, discovered by Count Bégouen in the Grotte des Trois Frères (French Pyrenees), featuring the cave cricket Troglophilus. (After Bégouen)

The Slovenian Olm, Proteus, seems to have been well-known to the villagers of the Trieste area for centuries. Specimens occasionally appeared after floods in the Lintverm (from the German ‘Lindvurm’, meaning ‘dragon’) – a tributary of the River Bela near Vrihnika. With their long, pink, rather reptilian bodies, they were taken, not unreasonably, to be dragon fry – the offspring of a shadowy monster who lived in the roaring cave from which the river flowed and who caused periodic floods by opening sluice gates when her living quarters were threatened by rising water. But in the 1680s, Baron Johann Valvasor, a Slovene nobleman and well-travelled amateur scientist, ruined centuries of colourful legend by exposing the Olm as a perfectly natural blind cave salamander.

In 1799, the German naturalist-explorer Baron Alexander von Humboldt, accompanied by a French botanist called Bonpland, visited the famous Cueva del Guacharo in the Caripe Valley of Venezuela. There he collected and described a cavernicolous bird, Steatornis caripensis, belonging to the order which includes the nightjars, which had been known for a long time to the Indians under the name ‘guacharo’. Humboldt was greatly impressed by the screeches produced by the birds when disturbed at their cave roost. “Their shrill and piercing cries strike upon the rocky vaults,” he wrote, “and are repeated by the subterranean echoes.” Having heard them myself, I would describe the racket as the sound of a thousand mad chickens locked up in a barn with a fox.

In 1808, Schreibers discovered the first invertebrate cave fauna in Austria and more extensive collecting was done in the Postojna area by Count Franz von Hohenwart and others from 1831 onwards. It was there too that the Danish zoologist J.C. Schiodte recognized that cave faunas showed differing degrees of specialization to life in darkness, and so laid the foundations for a system of ecological classification of cave life. This was advanced in a more rigorous form in 1854 by J.R. Schiner and has been widely used by cave biologists ever since. This work perhaps marked the beginnings of the systematic discipline of ‘biospȼologie’, a term proposed by Armand Viré in 1904, to refer to the study of subterranean life.

Fig. 1.8 The old route across the underground river Pivka in the Great Hall of Postojna Jama in Slovenia from an aquatint engraved by G. Dobler after a painting by Alois Schaffenrath, published in 1830. (Courtesy of Trevor Shaw)

In the USA important work continued intermittently from 1840. In that year Davidson collected the first specimens of a blind white fish in Mammoth Cave, described by de Kay, Wyman and Tellkampf as Amblyopsis spelaea. Tellkampf went on to describe other fauna from Mammoth Cave and was followed by E.D. Cope and A.S. Packard, whose remarkable studies through the 1870s put America for a time at the forefront of biospeleological research. Meanwhile, in the 1840s, V. Motschoulsky reported the first cave-specialized insects captured in the caves of Caucasia, and in 1857 De la Rouzee discovered the first cavernicolous insects known from France.

Scientific investigation of our cave faunas began in a round-about way in about 1852, when Professor Westwood and S. Bate included the following reference in their History of the British Sessile-eyed Crustacea, Vol.1, published in 1863.

“In the year 1852”, writes Bate, “Professor Westwood was so fortunate as to obtain from a pump-well near Maidenhead, a quantity of [Niphargus sp.] … since when they have been found in Hampshire, Wiltshire … and very recently in Dublin.”

Shortly afterwards, news of the discovery in Europe and America of strange blind cave animals prompted Naturalists E. Percival Wright and A.H. Haliday to search for similar creatures in Mitchelstown New Cave in Co. Tipperary. Their search was successful and they described their find – a tiny Collembolan doubtfully identified as Lipura stillicidii Schiodte – in a paper read before a British Association Meeting in Dublin in 1857.

More than thirty years were to elapse before the next glimmer of enthusiasm for Irish cave life manifested itself in the form of a joint excursion in 1894 by the Dublin, Cork and Limerick Field Clubs to the Cave of Mitchelstown. One of the participants, George H. Carpenter, recorded that “after an informal luncheon on the roadside, the party being provided with candles, descended the sloping passage and ladder which led to the depths below.” They spent two hours searching for cave animals and, although they failed to reach the underground river, made a reasonable collection of fauna, including the rare blind cave spider now known as Porrhomma rosenhaueri. In the same year, pioneering English arachnologist F.O.P. Cambridge collected spiders in Wookey Hole, but without finding anything of particular interest.

Early in 1895 E.A. Martel and his wife paid a well-publicised visit to Ireland. The event prompted the Fauna and Flora Committee of the Royal Irish Academy to support H.L. Jameson with a grant “to further investigate cave fauna in Ireland”. He joined the Martels in the Enniskillen area of Co. Fermanagh and, while the Frenchman surveyed the caves and drew up his plans, Jameson collected cave animals. The interest seems to have persisted, for Jameson is also known to have made faunal collections in Speedwell Mine in Derbyshire in 1901, but there then followed a gap of over thirty years during which British cave fauna was again neglected.

Fig. 1.9 One of the earliest illustrations of cave fauna from Adolf Schmidl’s Die Grotten und Höhlen von Adelsberg, Lueg, Planina und Laas. Wien, Braumüller, 1854. (Courtesy Trevor Shaw)

In 1936 the British Speleological Association was launched, with a brief to co-ordinate the work of caving clubs and to foster interest in the scientific aspects of caving. Things did not run entirely smoothly, however, and in 1947 another body, the Cave Research Group of Great Britain, emerged with a more specific research interest. Both societies ran in parallel until 1973 when they merged to form the British Cave Research Association which has become a major publisher of speleological research.

Meanwhile another organization concerned with cave science had been formed in 1962. This was the Association of the Pengelly Cave Research Centre, now the William Pengelly Cave Studies Trust. It is London-based, but its interests are very much centred in Devon where it runs the Pengelly Cave Research Centre at Buckfastleigh. The trust is active in education and conservation and produces publications covering a broad range of speleological topics.

The multidisciplinary nature of speleology allows significant contributions to be made as much by talented amateur observers as by trained professional scientists, and we owe much of our present knowledge of the faunas of British caves to the work of a handful of exceptionally dedicated amateur naturalists. The central figures of the group were Brigadier E.A. (Aubrey) Glennie and his niece Mary Hazelton, who in 1938 began making systematic collections in the caves of Yorkshire, Derbyshire and Mendip. Glennie, an excellent all-round naturalist, picked up his interest in cave life while serving in India, where among other things, he published a study on the nesting behaviour of Himalayan Swiftlets in caves. On his retirement in 1946, he became a driving force in the biological work of the newly formed Cave Research Group, and was soon recognized as an authority on British hypogean amphipods. Hazelton assumed the mantle of Biological Recorder to the CRG, and for the next 29 years diligently co-ordinated the identification of collections submitted by fellow cavers and compiled the results for publication, first in the Transactions of the Cave Research Group and later of the British Cave Research Association. Among the most notable contributors to the faunal collections of this period were Jean Dixon of the Northern Cavern & Mine Research Society and W.G.R. Maxwell of Chelsea Speleological Society.

The 1950s saw the appearance on the scene of two particularly influential figures, both professional biologists. One was Dr Anne Mason-Williams, a microbiologist whose pioneering studies on the microflora of South Wales caves remains the definitive work in this field. The other was Dr G.T. ‘Jeff’ Jefferson, a lecturer in zoology at University College, Cardiff, who quickly established himself as the leading authority on British cave faunas and went on to become president of the British Cave Research Association, and a greatly respected ambassador for speleology in Britain. Jefferson’s major contribution to cave science in Britain before his untimely death in 1986, was in shaping the wealth of observation gathered by his amateur predecessors into a coherent picture of the biogeographical history and ecological relationships of our cave fauna. It is his work above all that has provided the inspiration for this book.

Non-cavers are fond of asking cavers why they venture underground. The usual answer is along the lines that “caving is good fun”. Many would add that caving is most fun when spiced with the excitement of discovery. For the sporting caver, this means finding a way into previously unvisited passages, or whole new cave systems. For the speleologist there is the further excitement of recording new observations and of gaining fresh insights into the history, development, or life of the cave. The discipline of cave biology remains poorly developed in Britain and Ireland, affording tremendous scope for discoveries of all sorts by amateur as well as professional naturalists.

Driving curiosity and a sense of wonder are perhaps the two features which above all unite the caver and the naturalist. I hope that this book can make the passion of the one intelligible to the other, and so enhance the experience of both.

2

The Cave Habitat

What is a cave?

Put this question to any wetsuit-clad, hard-hatted individual found walking across the Mendip Hills, Yorkshire Dales or the shining limestone pavements of the Burren, and you will discover that a cave is a naturally-formed hole in limestone which is large enough to be explored by a caver.

Ask the same caver what he or she has noticed in the way of living creatures in caves, and the answer may well be “not a lot.” It will perhaps surprise most cavers (and naturalists) to learn that over a hundred species of invertebrate animal have been recorded as maintaining permanent populations in cave habitats in Britain and Ireland, plus another score or so species of creatures such as bats and moths which use caves as a regular part-time shelter. The cryptic community to which these creatures belong remains largely undetected by cavers because it generally avoids the relatively large tunnels and booming chambers, the glistening calcite draperies and crashing waterfalls which so captivate the human cave enthusiast, preferring instead the cosy confines of smaller cracks and crevices. I hope in this book to shed light on at least a portion of this unsuspected world which lies beneath our feet, whether we live in Grassington or Glasgow, Lisdoonvarna or London, and to offer pointers to fellow amateur naturalists towards fruitful areas of investigation for the future.

To unravel the natural history of a cave, or indeed any habitat, we must try to perceive it as far as possible from the point of view of its inhabitants. It requires a considerable effort of imagination for such sight-dependent creatures as ourselves to grasp the essence of life in the dark and labyrinthine realm of the cavernicole. A little inspired speculation may be needed to find the ‘right’ questions to lead us to fresh insights into the mysterious world beneath us.

We might start by imagining what kinds of habitats could be accessible to the cavernicole and then consider which environmental characteristics of such places are likely to influence its choice of where to live. Almost at once we run into problems, for although a good deal is known about the environment in man-sized, air-filled limestone caves in Britain and Ireland, we know much less about the conditions within smaller cracks and crevices or in caves beneath the water-table, and less still about our submarine caves. Fortunately, such information is more readily available from other parts of the world. So in this chapter we will take an international approach to defining and classifying the cave environment, before turning in later chapters to a detailed consideration of what is known about our own cave fauna.

What then is a ‘cave’ as perceived by its inhabitants? The dictionary definition of “a natural underground chamber” gives us a less than helpful starting point, for why should we suppose that the cavernicole will distinguish between natural or man-made tunnels, or between subterranean and above-ground enclosed chambers, as long as the appropriate conditions of food supply and microclimate are present in the living space? Should we then include mines, adits, buried pipes, culverts, sewers, cellars, tombs, the London Underground System, or perhaps even houses and other enclosed buildings in our preliminary list of potential cave-habitats? To what extent should our definition specify the material bounding the cavity? Must a cave be rock-lined, or should we widen our brief to include animal burrows and other spaces present in soil, for surely it must be arbitrary to distinguish between an earthy burrow and a muddy hole of similar dimensions in rock?

Fig. 2.1 The main tunnel of Sleets Gill Cave in Wharfedale, Yorkshire Pennines – a classic phreatic tube, formed and enlarged by water filling the passage and so dissolving the limestone rock equally on all sides. (Chris Howes)

As it happens, soil faunas are very well documented, and while it seems that many animal groups are common to both soils and caves (and indeed to leaf-litter and the deep moss-carpets of tropical regions as well), the fauna of organically-rich topsoils is sufficiently distinct from that of most rock-space habitats to warrant a separate treatment. I shall therefore exclude soils forthwith from our definition of cave habitats (but see ‘Cave sediments’ under ‘Types of cave habitat’ later in this chapter). Similarly, the voids in other organic, living or once-living materials, such as wood or the guts or blood vessels of animals, have distinctive specialized faunas of their own, clearly distinguishable from those of habitats within inorganic materials – although some specialized xylophages, such as termites, and endoparasites, such as tapeworms or flukes, share certain morphological specializations (eyelessness, depigmentation) characteristic of the more specialized cavernicoles. When it comes to holes of human fabrication, most significant biological criteria must lead us to include them in our category of caves. That they have a very poor fauna in comparison with natural caves, is due less to their artificial nature than to their frequent isolation from sources of natural colonization and their often unfavourable microclimate.

Having narrowed our definition of the cave environment to ‘habitable voids bounded by walls of rock, or similar inorganic materials’, let us now consider the physical criteria which may determine their habitability: the presence or absence of light, physical space (the size of the hole), the medium filling the space (water or gas mix), the microclimate within the medium (the pattern of change in temperature, pH, etc. over time), and the nature and amount of available food.

Let us begin with the business of light, a variable of obvious biological significance. Beyond the limits of light penetration, the cavernicole will be obliged to rely on senses other than sight, and on foods other than green plants. Perpetual darkness is a characteristic of most rock void habitats anyway, so let us choose to define ‘the cave’ as a habitat entirely without natural illumination. This will substantially simplify our task, by excluding from the cave fauna a whole host of organisms which seek shelter in cave entrances, but also live in a wide range of other shady, sheltered habitats such as the woodland floor, or river gorges, or houses and other structures used by people. Later we will consider the illuminated portions of man-sized caves as a significant ‘cave-related habitat’ – the ‘cave threshold’ – simply because it is familiar and accessible to cavers, while ignoring all other lit, cave-related habitats.

In the world of dark holes, the physical dimensions of a potential habitat are of obvious importance in determining what creatures can colonize it. One has only to consider the relative body-diameters of a man (say 450 mm across the shoulders), a Greater Horseshoe Bat (60 mm), a cave spider such as Meta menardi (6 mm), a springtail (0.6 mm) or a nematode worm (0.06 mm) to appreciate that one creature’s spacious accommodation may be another’s unenterable squeeze, and that the cave biologist may be excluded physically from all but a tiny proportion of the very largest of cave habitats. Frank Howarth, an entomologist who works mainly on the fauna of Hawaiian lava caves, distinguishes three principal hole-size categories which appear to have biological significance for subterranean biotas. He terms these ‘macrocavernous’ (>200 mm diameter), ‘mesocavernous’ (1–200 mm diameter) and ‘microcavernous’ (<1mm diameter).

The characteristic inhabitants of Howarth’s microcaverns are sometimes termed ‘the interstitial fauna’. They include a distinctive suite of specialized, skinny-bodied crustacea (such as Bathynella and various harpacticoid copepods) and other tiny creatures (such as rotifers, nematodes and tardigrades) which mostly like to be in contact with a solid surface on all sides and typically inhabit the spaces in between unconsolidated, fine-grained sediments such as the sand and gravel of river beds and the seashore. I propose, on purely arbitrary grounds, to exclude this fauna from further discussion in this book (except for species which also frequently inhabit larger spaces), and to restrict the definition of the cave habitat to holes of 1 mm diameter upwards, that is, to mesocavernous and macrocavernous habitats.

Various vertebrates use macrocavernous caves (and the larger mesocaverns) for shelter and they, and the other species which depend on their presence, form characteristic communities which reach astonishing levels of diversity and abundance in tropical regions. I shall long remember my first visit to the spectacular Deer Cave in the Gunung Mulu National Park in Sarawak, where at dusk close on half a million bats stream out of the cave in a seemingly-endless cloud which winds its way across the sky with a rush of wings like the sound of Niagara Falls. British bat-watchers have to be content with the odd flap, but in spite of declining populations, cave-roosting bats are still widespread and bat caves do support their own suite of associated ‘batellite’ cavernicoles. Other cavernicoles may, for example, be specifically associated with the guano of cave-roosting crickets, or with cave sediments introduced by sinking streams.

Mesocavern-sized holes not only occur within karstic rocks, but also in screes, in the coarse gravels and rocky beds of upland rivers, between the pebbles and cobbles of exposed sea-shores, in the fractured zone of non-karstic rocks (especially shales) just beneath the soil, and as cooling cracks in lava flows and other igneous rocks. They represent a very much larger habitable subterranean space than do macrocaverns and so have developed a richer and often more specialized fauna, frequently dominated by species peculiar to this habitat and characterized by a reduction in the size of the eyes, loss of pigment and various other specializations. These ‘mesocavernicoles’ may also occur in soil spaces, or animal burrows, or even in large macrocaverns, provided there is an adequate food supply of down-washed organic material and a fairly stable humid microclimate. Not all species within the mesocavernous fauna will be found in all related habitats; some do not seem to occur in soil-spaces, others shun human-sized caves.

Simply as a consequence of our own species’ enormous body-size, we are physically excluded from the very habitats which are most likely to harbour a specialized fauna. In the absence of appropriate tools with which to peer inside mesocavernous habitats, cave biologists have so far been forced to infer what they can about them from the behaviour of their biotas where they pop up in the accessible portions of people-sized caves. These act as windows into the mesocavernous world, but it seems likely that they provide a distorted view, encouraging widely differing interpretations of the nature of what has been observed. The present situation in cave biology is a bit like that which prevailed among astronomers a century or so ago, when dependence on inadequate earth-based optical telescopes sustained the widely-held belief that Mars was criss-crossed by an elaborate network of irrigation canals built by Martians. Speculation and controversy abound no less in cave biology literature, while cavernicolous communities remain enigmatic and under-recorded. As a result, new species await discovery in most subterranean habitats in every part of the world including the British Isles. In short the whole subject of cave biology is very much still in its infancy. A nice illustration of this turned up on my desk in the form of a report from Frank Howarth, announcing his discovery of a brand-new diverse fauna of highly specialized cavernicoles in lava caves in tropical Australia. For years Australia was thought to have a very poor fauna of specialized cavernicoles, and a number of papers sought to explain this on theoretical grounds. For example, it was argued that Australia’s climate during the Pleistocene had not been harsh enough to exterminate the above-ground populations of its cavernicoles, and so any tendency on their part towards specialization for underground life would be continually cancelled out by gene flow from outside the cave. Having wickedly sub-titled his paper Why there are so many troglobites [= highly specialized cavernicoles] in Australia, Howarth makes the telling point that “One has to actually enter a cave and look for troglobites before proclaiming on theoretical grounds that none could exist.” I offer this creed to the reader in the context of the British cave fauna. Let us, as naturalists, devise ways to find out what lives in our underground world and get down and study it at first hand.

I have distinguished between ‘interstitial’ (microcavernous) and ‘cave’ (meso- and macrocavernous) habitats on the grounds that their biotas are substantially distinct. We might expect a similar distinction to exist between ‘aquatic’ and ‘terrestrial’ cave communities. Certainly, there are some cavernicoles which are essentially aquatic, and others which are essentially terrestrial. However, the atmospheres of most mesocavernous, and of some macrocavernous, gas-filled habitats are permanently saturated with water vapour. This poses physiological problems for many groups of terrestrial arthropods which, unless equipped to eliminate excess water from their tissues (as aquatic species do), would quickly die of ‘water poisoning’ through dilution of their body fluids. Not surprisingly, ‘terrestrial’ mesocavernicoles have been found to be physiologically specialized to cope with a hydrating atmosphere and seem able to withstand long periods of immersion in freshwater – an adaptation which is essential in habitats which are frequently flooded by downward-percolating rainwater or by fluctuations in the water-table. Some seem equally at home in air or water, and can frequently be seen feeding on the floor of cave pools among their aquatic counterparts. Conversely, many freshwater aquatic mesocavernicoles seem able to cope with ‘terrestrial’ life without undue physiological stress and have been recorded as living out of water for several weeks at a time. So we see that the distinction between terrestrial and freshwater aquatic cave habitats is not exactly cut-and-dried, although there is a clear distinction between the communities present in either zone and those found in marine cave habitats.

Not all terrestrial cave habitats are moist. Large caves with more than one entrance often experience drying airflows which can produce desert-like conditions which are lethal to the hygrophilic denizens of the mesocaverns. However, such caves are often easily accessible and attractive to vertebrates, and may (especially in the tropics) support vast populations of bats, birds and guano-associated invertebrates. Guanobious animals exhibit few or none of the morphological characteristics considered by European cave biologists to be the mark of a ‘true cavernicole’ or ‘troglobite’, yet they may be just as exclusively cave-dwelling as any mesocavern specialist. Above-ground human structures are usually designed to be as dry as possible and are seldom completely dark, and this makes them suitable as a habitat for only a very few cave-threshold specialists, such as the daddy long-legs spider Pholcus phalangioides which presumably originated somewhere in the Mediterranean region, but in the UK is found only in houses. In between the dry, draughty macrocaverns and the soggy, airless mesocaverns, there may be wide expanses of transitional cave habitats with a variable microclimate, posing a distinct set of problems for the communities which inhabit them. Terrestrial inhabitants of such places must cope with the physiological stress of desiccation some of the time and physiological drowning for the rest of the time. In the tropics, transitional cave habitats may be particularly extensive, with their own specialized faunas, often dominated by ‘bandits’ – marauding predators and scavengers which live off the scraps of the guano-based community. Climatically similar conditions are found in man-made culverts and other artificial tunnels, and these frequently attract transitional-zone cavernicoles such as the widely distributed cave spider Meta menardi. Later we shall distinguish a range of natural and artificial cave habitats principally on the basis of their microclimatic regimes.

In earlier discussing the criteria which may be important to cavernicoles in choosing their habitats, I included the apparently pedantic phrase ‘gas mix’, rather than ‘air’ in my list of the media which may fill mesocavernous voids. I did so because it seems that the atmosphere of mesocaverns may differ substantially from that found in open macrocaverns with a good air circulation (which generally have much the same atmosphere as the outside world). Bacterial decomposition of organic material in small spaces frequently results in unusually high atmospheric concentrations of carbon dioxide. Frank Howarth’s new Australian cavernicoles, mentioned earlier, were found in poorly ventilated lava caves which are thought to share the atmosphere of the mesocavernous spaces in the surrounding basalt. The air in these caves is saturated with water vapour and contains around 250 times more carbon dioxide than normal air. Bad air caves occur in Britain too, but have not yet been biologically investigated.

Finally, we may seek to distinguish cave habitats from non-cave habitats in terms of their food supply. Early cave biologists, whose experience of cave faunas was mainly confined to the larger, more easily explored ‘fossil’ macrocaverns (those no longer bearing the watercourses which formed them) of temperate European limestone areas, concluded that cave animals were perpetually starved. While food resources may be very thinly distributed in such cave habitats, in others (and particularly in the tropics) food may be superabundant. The biotas of food-poor caves are adapted to eke out what little energy is available, while those of food-rich caves are adapted to a life of plenty. Caves may contain a wide range of food sources, including living vegetation (tree roots, saprophytic plants and fungi which get their energy by digesting organic matter rather than by trapping sunlight, fruits carried in by vertebrates), living invertebrate or vertebrate animals, and all kinds of detritus. Cavernicoles may be plant-, fungus-, detritus- or bacteria-feeders, predators, parasites or a combination of these. In short, caves are more ecologically diverse than most biologists realize.

To summarize then, cave habitats may be defined as ‘perpetually-dark voids, more than one millimetre in diameter (and sometimes much larger), bounded by rock or similar inorganic materials, and filled with gas (‘fresh’ or ‘bad’ air) and fresh or salt water.’ Within such habitats, the microclimatic regime and the type and quantity of the available food-supply largely determines the species composition of the cave community. Only the largest (and often, in our islands, the least populated) cave habitats are accessible to human observers, so that we know a good deal less about the composition and functioning of cave communities in Britain and Ireland than we do about most other natural communities of our islands.

What lives in caves?

Of the voluminous literature dealing with the biota of caves, two works of this century stand out for sheer scope of vision. The first, B. Wolf’s Animalium Cavernarum Catalogus, published in three parts between 1934 and 1938, lists all animal species recorded from caves to that date. The second, by A. Vandel, published in French in 1964, discusses the biota and biology of caves worldwide. An English translation, published by Pergamon Press in 1965 as Biospeleology: The Biology of Cavernicolous Animals, is perhaps still the most useful general text despite its wacky view of evolution in caves. L. Botosaneanu’s book Stygofauna Mundi, published in 1986, gives a more up-to-date account of the fauna of subterranean waters, but there is need for a similar treatment of the terrestrial cave fauna to take into account the spate of biological discoveries in tropical caves during the decade and a half since Vandel’s book. The following brief summary illustrates the range of life forms presently known to inhabit caves.

Fig. 2.2 Leptodirus hohenwarti, a highly cave-evolved beetle discovered in 1832 by the Count von Hohenwart in the Slovenian cave of Postojna Jama.

Kingdom MONERA

Phylum Bacteria

Well represented in caves. Includes saprophytes, pathogens and chemoautotrophs (which live by oxidizing or reducing iron and sulphur compounds). Bacteria are at the base of many cave food-chains.

Phylum Cyanobacteria

Some species are capable of synthesizing their pigments in the absence of light. Various Chroococcaceae are implemented in the formation of complex cave mineral deposits such as moon milk and tufa (see glossary).

Kingdom PROTISTA

Phyla Phytoflagellata, Zooflagellata, Sarcodina, Ciliophora, Sporozoa

Protista are often abundant in interstitial waters and many species occur in caves. In Turkmenistan, brackish wells in the Kara-Kum desert contain abundant populations of at least 10 species of unusually tiny, thin-shelled Foraminifera. Cave clays often contain Mastigophora, Sarcodina, Amoebina and some Ciliata.

Kingdom PLANTAE

Phylum Chlorophyta

Various free-living algae, such as Chlorella, Scenedesmus and Pleurococcus are found growing deep inside caves. Though able to synthesize pigments in the dark, they appear to use non-photosynthetic metabolic pathways. The other plant phyla Rhodophyta, Phaeophyta, Bryophyta are essentially absent from the dark parts of caves. The phylum Tracheophyta is represented by a very few aberrant saprophytic species which can live independently of sunlight.

Kingdom FUNGI

Phyla Zygomycetes, Ascomycetes, Basidiomycetes, Myxomycetes

Fungi are important in cave ecosystems. Most are saprophytic on organic material washed into caves and form the main food base of cave communities. Some are epizoic (live on the outer surface of animals) or parasitic. Most members of the phylum Oomycetes are parasitic on flowering plants and therefore not represented in caves.

Kingdom ANIMALIA

Phylum Porifera

Encrusting sponges may be the commonest organisms in tidally flushed submarine caves.

Phylum Coelenterata

Hydra viridissima occurs in groundwaters in the Southern Carpathians of Europe. Marine Hydrozoa and Anthozoa are commonly found in submarine caves.

Phylum Platyhelminthes

Rhabdocoel Turbellaria are common in wells, springs and groundwaters. Cave-evolved Triclads have a worldwide distribution, with most species within three planarian families: Dendrocoelidae, Kenkiidae and Planariidae.

Phylum Nematoda

Free-living nematodes are frequent in groundwaters, caves and mines worldwide. Several freshwater species of the otherwise exclusively marine Desmoscolecidae inhabit caves in Slovenia.

Phyla Nemertinea and Rotifera

A few species of these small creatures inhabit interstitial waters and caves.

Phylum Annelida

Submarine caves often contain huge populations of sedentary polychaete worms and a number of cave-evolved freshwater polychaetes are known from Switzerland, Slovenia, Japan and Papua New Guinea. Oligochaete worms are often abundant in caves, in groundwaters and sediments. The family Lumbriculidae contains many essentially cavernicolous species. Cavernicolous leeches are known from Central Europe and several tropical countries.

Phylum Mollusca

There are many cavernicolous Gastropoda within the families Auriculidae, Zonitidae, Subulinidae, Enidae and Valloniidae (terrestrial species), and Hydrobiidae (aquatic species). The Bivalvia include cavernicolous species of Pisidium and Congeria in Europe and Japan.

Phylum Onychophora

The South African species Peripatopsis alba is known only from caves.

Phylum Arthropoda

Subphylum Crustacea

Class Remipedia: Recently discovered in submarine caves in the Bahamas and Canary Islands, these actively swimming predators resemble aquatic centipedes.

Class Ostracoda: There are many groundwater species, some of which also occur in larger caves.

Class Copepoda: Many cyclopoids and harpacticoids occur in caves and interstitial groundwaters worldwide.

Class Malacostraca: The monospecific order Spelaeogriphacea is so far known only from caves in South Africa. Thermosbaenacea and Mysidacea are widespread in submarine caves and brackish groundwaters and a few species have made the evolutionary shift into freshwater caves. Isopoda are one of the best-represented orders in the subterranean world, with hundreds of cavernicoles described within the Asellidae and Oniscoidea. The Amphipoda, notably the Gammaridae, are equally well represented. Cavernicolous decapods such as crayfishes, galatheids, crabs and river prawns are particularly widespread in the tropics. Groundwater-inhabiting members of this class often belong to ancient lineages and the distributions of related taxa provide important evidence in reconstructing the history of the planet.

Subphylum Uniramia

Class Diplopoda and Pauropoda: Worldwide there are hundreds of species of cavernicolous millipedes, and particularly of Polydesmoidea. They often show relictual distributions which mirror past configurations of the earth’s crustal plates, long since redistributed by seafloor spreading and continental drift. A few Pauropoda are known from caves.

Classes Chilopoda and Symphyla: Cavernicolous Scolopendromorphs and Lithobiomorphs are known from European caves. In the tropics there are also cave-evolved Scutigerids. The Symphyla live in the soil and look like cave animals, but most feed on living plant roots and so are excluded from deep cave habitats.

Class Insecta: The Collembola and Diplura are primitive, wingless, ground-dwelling insects which require a high humidity. They include a large number of cave-evolved species worldwide. Cavernicolous Blattodea are mostly confined to the tropics. Within the Orthoptera, the Rhaphidophoridae or camel crickets contain a number of conspicuous cavernicoles with a worldwide distribution and a few cavernicolous gryllids are found in the tropics. There are cave-evolved Dermaptera, Psocoptera, Hemiptera, Trichoptera, Lepidoptera and Diptera. Not surprisingly, the majority of cavernicolous insects belong to the largest order and the most successful group of animals on earth, the beetles (Coleoptera). At least 22 families contain cavernicoles, which reach their greatest diversity and specialization in the Trechidae and Leiodidae.

Subphylum Chelicerata

Class Arachnida: A few cavernicolous Scorpiones, Uropygi, Amblypygi, Schizomida, Ricinulei and Palpigradi are known from tropical regions. Pseudoscorpions are well represented in caves, with over 300 cavernicolous species, many of which are giants among their kind, with very long legs and claws. The Opiliones also contain cavernicoles, most notably in the families Phalangodidae, Travuniidae and Ischyropsalidae. The terrestrial mites (Acari) most frequently found in caves are tiny Gamasides within the families Parasitidae, Rhagidiidae and Eupodidae and there are many cavernicolous water mites in the families Hydrachnellae and Porohalacaridae. Spiders (Araneae) dominate the predator niches in most tropical caves and include hundreds of cavernicolous species worldwide. In temperate regions, the most specialized cavernicoles belong to the primitive families Dysderidae, Leptonetidae, Telemidae and Oonopidae, but there are also many specialized species of Linyphiidae, Erigonidae and Agelenidae.

Fig. 2.3 Neobisium spelaeum, a giant cavernicolous pseudoscorpion which preys on the cave beetle Leptodirus hohenwarti (shown in Fig. 2.2)

Phyla Tardigrada and Bryozoa

A few species inhabit groundwaters.

Phylum Echinodermata

Various detritivorous brittle stars (Ophiuroidea) and sea cucumbers (Holothuroidea) frequently occur in submarine caves, but no strictly cavernicolous species are known.

Phylum Chordata

Class Teleostomi: Freshwater cavernicolous fishes are found mainly in the more arid regions of the world. To date around 60 more or less blind and depigmented species representing 8 orders and 13 families have been collected in freshwater and submarine caves, springs and groundwaters. The most speciose families are Cyprinidae, Gobiidae and Bythitidae, followed by Pimelodidae, Characidae, Cobitidae and Amblyopsidae.

Class Amphibia: 14 species of cavernicolous Urodela are known from North American caves and one from Europe. The latter, Proteus anguinus was the first cavernicole to be recognized as such. In common with species of the American genera Gyrinophilus, Eurycea, Typhlomolge and Haideotriton, Proteus retains larval gills in the adult stage, and is thus able to live permanently beneath the water table.

Class Reptilia: The colubrid snake Elaphe taeniura is a common inhabitant of caves in south-east Asia, from China to Borneo, where it preys on bats and swiftlets.

Class Aves: While no birds live permanently in caves, swiftlets of the genus Aerodramus (Apodidae) and the oilbird Steatornis caripensis (Caprimulgidae) are dependent on caves as nesting sites and are capable of navigating long distances underground and in total darkness by echolocation using ultrasonic clicks.

Class Mammalia: It is possible that a South American mouse Heteromys anomalus and one or two species of tropical shrews in the genus Crocidura may establish permanent cave populations. Many bats (e.g. Tadarida spp.) are dependent on caves for shelter, but none are cavernicolous.

In summary, although green plants are largely absent from caves, cavernicolous species are found within most of the major classes of animals, and are particularly common among the Crustacea, insects, spiders and millipedes.

Caves in limestone

Of several cavernous rocks in Britain and Ireland, one above all others provides extensive integrated cave systems of a size which allows the biologist to study the life they contain with relative ease. It is the Carboniferous Limestone.

Fig. 2.4 The blind North American cave fish Speleoplatyrhinus poulsoni has an extraordinarily developed lateral line system, with correspondingly enlarged brain parts for processing tactile and positional information.

The cave-bearing limestones are concentrated in six major patches: in County Fermanagh (the largest, but least well prospected area), the Northern Pennines, Derbyshire’s Peak District, County Clare, Somerset’s Mendip Hills and South Wales. In the Northern Pennines alone, there are 1800 or more documented cave entrances and around 350 km of explored and mapped cave passages – while current estimates give the total length of mapped passages in Britain and Ireland at somewhere around 800 km. Cave exploration is still in a very active phase in these islands, and significant new discoveries are still being made. For example, recent explorations in Ogof Daren Cilau beneath Mynydd Llangattwg in South Wales have yielded over 20 km of new discoveries in less than two years, including the largest passages yet found in Britain.

By any standards, 800 kilometers of open cave passage represents a significant habitat, worthy of the attention of naturalists – yet passages of explorable size must form but a tiny proportion of the total cave habitat, the vast majority being of mesocavernous dimensions. In the absence of data, I would guess that the habitable surface area within the mesocaverns of limestone terrains must run to at least two or three orders of magnitude more than that within explored caves.

So what is it which makes limestones so spectacularly cavernous? To understand the process in which caves are formed, we must begin by examining the origins, nature and structure of the limestone rock itself. Limestone is a sedimentary rock, that is, it began life as suspended particles in an ancient sea, gradually settling to the ocean floor millimetre by millimetre over millions of years. During this inconceivably long period, there were intervals when conditions changed enough to interrupt the steady downward rain of lime, allowing some other type of deposit to intervene briefly in the sequence of otherwise pure calcium carbonate. Aeons later, and now hardened to rock, these geological glitches have become ‘fossilized’ as bedding planes – horizons of weakness between the solid layers of limestone.

The Carboniferous Limestones of the British Isles were laid down somewhere in the tropical seas of the southern hemisphere. Pushed along on a northward-drifting chunk of continental crust, they have had a bumpy ride. Some, like those of the Yorksire Dales, have survived their 340 million year journey the right way up, though somewhat fragmented by massive vertical faults. Others have fared less well. The Mendip limestones lie like a wrecked car, buckled and perched at a steep angle, so that the bedding planes dip downhill at an average gradient of 50° or so. In all cases, the rough ride has produced vertical stress cracks, called joints, which link with faults and with the original bedding weaknesses of the limestone to form a boxwork of crevices reaching from the highest hilltop to beneath the deepest valley.

Limestone is a strong rock and so frequently forms upland regions. Solid limestone is impervious to water, but water is able to flow through the cracks within it. It is these cracks which are the key to understanding the origins of caves. Limestone caves form principally by means of a simple chemical reaction in which hydrogen ions from groundwaters, acidified with dissolved carbon dioxide, act on the relatively insoluble carbonate ions in the limestone to produce soluble bicarbonate 10ns which are then flushed away. The reaction renders the limestone 25 times more soluble than it would be in pure water and the result is holes.

Some of the carbon dioxide in groundwaters is collected by raindrops falling through the atmosphere, and some from the breakdown of organic material picked up as the rain then trickles down through the soil. Immediately beneath the soil, the weathered surface layers of rock are more fractured than those at a greater depth and the acidified, aggressive soil waters have their maximum impact here – so that at any one time, up to 15% of the volume in the top three metres of limestone may be occupied by air-, or water-filled spaces (Stearns, 1977 – figures for Central Tennessee, USA). These mesocaverns act like the guttering beneath the roof of a house – collecting soil water and quickly conveying it to natural drainpipes, often developed on the intersections of major joint fractures, or steeply inclined bedding planes.

The flow of water downwards into the limestone carries with it sediments which contain particulate organic material, dissolved organic acids and microorganisms (bacteria and fungi). Decomposition continues way below the soil in the cracks and crevices of the limestone. There, to paraphrase Hoover’s famous advertising slogan, groundwater micro-organisms ‘eat-as-they-seep-as-they-clean’, mopping up the organic impurities and excreting CO₂ – in effect arming their liquid medium with chemical teeth. In the larger conduits it may take up to 50 days and several kilometres of flow before the bacteria finish mopping up the water-borne food, and even longer and further before the chemical aggression of the cave water is finally spent. All this time, limestone is being steadily corroded, and the cracks along which the water travels widened, resulting in the slow opening of a complex drainage network reaching deep below the water table.

The initial pattern of flow within the flooded cracks is dictated by the structural geology of the limestone and the shape of the land surface. Between them, these two factors determine where water will escape from the rocks as a spring, and lay down the blueprint for the caves to come. If the rock strata lie horizontally, as they do in the Yorkshire Dales, water is forced to follow a rectangular course down vertical joints and along short sections of horizontal bedding, producing the characteristic stepped profile of a ‘pothole’ system. If the strata are inclined, as in the Mendip Hills, drainage will alternate between short joint-controlled shafts and longer bedding-plane slopes, producing caves with a steep profile, but few vertical sections.

At or below the water table, the course taken by percolation water is determined by the direction of the hydrological gradient between where the water goes into the permanently-flooded system of cracks known as the ‘phreas’ and where it comes out again as a spring. Within the phreas, water is free to follow along, down or up the 3-D maze of cracks to produce the smoothest possible overall flow. Where the rock beds lie horizontally the smoothest profile may be along just one bed, producing a horizontal cave which may run for several kilometers (Yorkshire has many such systems). Where the rocks dip steeply in a direction which does not coincide with the hydrologically-determined direction of flow, the groundwater may be forced into a series of vertical z-bends, down joints and up the bedding, to tack its way to the spring (a classic example is Wookey Hole in the Mendip Hills). Where the limestone beds are trapped in a syncline or U-bend beneath impermeable rocks, water may be forced to travel down to great depths following the configuration of the rock strata. Chinese geomorphologist Yuan Daoxian has recently reported the discovery of a substantial cave at a depth of 2900 m below the water table in the Sichuan Basin in China. When perforated by drilling, the hole gushed water. Caves at this depth are, however, extremely rare and probably have little or no biological significance.

As the profile of the cave takes shape, under the twin controls of hydrology and geology, the ‘best route’ is inevitably favoured with a greater rate of flow, which promotes more rapid corrosion of its boundary walls – which in turn results in a still greater flow capacity. In this way, the initially diffuse drainage within the limestone is gradually simplified with increasing time (and depth) into a pattern of coalescing collectors of increasing diameter. Over the aeons, the vagaries of geology and hydrology may conspire to favour one particular route in preference over all others, opening it out to form a major trunk conduit which drains the entire subterranean aquifer to its spring, or ‘resurgence’.

I have suggested so far that cracks in the limestone can be enlarged to form mesocavernous conduits by corrosive water trickling gently down towards the water table under the influence of gravity, or by slow creeping but aggressive groundwaters draining towards a resurgence. However, chemical solution is not the full story – once the cave becomes large enough to be an efficient drain, fast-moving waters can carry sharp-edged grit, adding physical claws to chemical teeth. Grains of quartz (a mineral much harder than calcite) provide a particularly effective scouring agent, and are easily collected by streams running over the Millstone Grit which butts onto much of our cavernous limestone. Where such a stream is captured by a well-developed Yorkshire joint, the outcome is a vertical pothole; on Mendip, an inclined swallet cave results.

Erosion of the river valleys which drain a limestone block may lower the water table within it, so that a conduit formed within the flooded phreas eventually becomes emptied of water and filled with air. One such system, GB Cave in the Mendip Hills, has received intensive study in recent years – in turn by Drs Tim Atkinson, Pete Smart and Hans Friederich of Bristol University. Their work has demonstrated the extent and importance of the system of mesocavernous conduits which overlies and feeds water and sediment into GB Cave. The conduits can be divided into three types. First there is the dense network of ‘subcutaneous’ cracks in the top three metres of rock beneath the soil. These have a large total volume and drain rapidly into the underlying cave, via mesocavernous collectors. They operate intermittently for up to two days following rain, but do not store a great deal of water. Two other types of inlets feed into the cave. They are small-diameter seeps, which stay full of water all the time and show little variation in flow discharge (flow being constrained by their small diameter); and vadose flows, which have higher and more variable discharges than do the seeps. Smart and Friedrich report that inlets are more frequent into shallower cave passages, and less frequent at depth, but do not give estimates of the porosity represented by these inlets, for which we have to consult Stearns on his Tennessee karst. Thus, at 10 m depth, the initially high porosity within the zone of subcutaneous flow (15%) may have fallen to about 1.5%, with a mainly downward flow via mesocavernous shafts and vadose cracks. At 30 m depth, porosity is down to 0.002%, and flow (at least in massively-bedded limestones) is increasingly confined within macrocavernous collector passages, fed by a converging network of smaller collectors of mesocavernous size. Thus, the main concentration of cave habitats (of mesocavernous dimensions) lies within the top three metres of bedrock.

Fig. 2.5 The main streamway in Poulnagollum Pot, Co. Clare – a classic vadose passage cut down through the limestone beds by an allogenic stream flowing off the eastern flank of Slieve Elva (compare with Fig. 2.1). (Chris Howes)

Phreatically-formed passages can be recognized by their characteristic circular or at least symmetrical cross-section, produced by equal corrosion of the walls, ceiling and floor (a classic example is Peak Cavern in Derbyshire). As soon as they develop an air surface, corrosion and erosion become channelled downwards and the cave stream begins to cut a trench into the floor, as is seen in the Ogof Ffynnon Ddu streamway in South Wales. This may eventually result in a canyon-shaped passage many metres deep.

As the cave matures, the enlargement of joints and bedding planes may weaken whole blocks of the ceiling and floor, resulting in their collapse. Where the cave contains an aggressive stream, such material may be removed as it falls, creating a chamber whose size is limited only by the structural strength of the overlying rock. Given enough time, the roof will eventually fail, opening the cave to the sky; if the collapsed blocks are not removed by water, the cave fills up with rubble.

The same chemical process which resulted in the removal by solution of limestone in cracks close to the surface, can go into reverse when acidified, lime-laden waters drip through cracks into an underground passage full of fresh air. As CO₂ in the hanging water droplet diffuses out into the air of the cave, the resulting transformation of bicarbonate to carbonate ions forces lime to precipitate from solution. The drip falls, a rim of lime remains on the cave ceiling, and hey presto, a few thousand years later the cave is festooned with sparkling stalactites. Given an aeon more, these may completely fill up and block the passage.

Caves may also become filled with insoluble sediments from outside. This is frequently the case in Britain, where sediments enter the cave by one of three main mechanisms: large masses of unsorted clay-and-rubble have slumped into caves as a half-frozen mush during the glacial advances of the Pleistocene; sands and gravels are washed in by cave streams and dumped as the waters slow down in more gently graded stretches of cave; and fine mud is often trickled downwards by percolation water until it completely fills passages right up to the roof.

The worst ravages of collapse and sedimentation may be reversed by a little-known bio-chemical phenomenon known as ‘digging’. First noted in Mendip caves, it appears to be caused by large sweaty men in overalls, armed with plastic buckets, and generally takes place at weekends in the pursuit of new explorations and discoveries underground. The chemical component of the process consists in a sparing application of ‘Dr Nobel’s Linctus’ to otherwise immovable blockages, with sometimes impressive results. We shall consider the conservation implications of digging and blasting in caves in a later chapter.

Types of cave habitat

In the previous section, we traced the process of cave formation in limestones by the gradual chemical enlargement of bedding cracks and joints, their subsequent drainage, further enlargement, collapse and infilling by sediment, breakdown and speleothems. In the course of this ‘life cycle’, limestone caves present a series of distinct habitats which are each exploited by a characteristic biota.

In recent years, similar biotas have been found in equivalent habitats in a wide range of other rocks (lava, gypsum, mudstone, shale, chert, breccia, tuff, rhyolite, diorite, quartzitic sandstone, etc) and sediments. This has led to a plethora of exotic technical terms in the literature – it seems that any biologist who finds a new habitat wants to give it an impressive, polysllabic label, an urge doubtless born of years of grappling with latin species names. My favourite examples include ‘parafluvial nappes’ (as worn by water-babies?), ‘hypotelminorheic biotope’ and ‘the petrimadicolous biocoenose’ (etymologically-inclined readers may enjoy trying to sort out these little beauties). In the section which follows, I have attempted to keep things simple by stressing the the similarities between habitats, rather than the differences between them.

Fig. 2.6 Cave habitats and structural features in a limestone upland.

1. Dolines or shakeholes 2. SUC or subcutaneous zone 3. Mesocavernous seeps and conduits 4. Air-filled macrocavern or dry cave passage 5. Vadose macrocavern or wet cave passage 6. Rimstone gour pools 7. Cave sediment 8. Breakdown blocks 9,10. Riffle and pool in cave system 11. Perched siphon or sump 12. Water table 13. Water-filled macrocavern or sump in the phreas below water table 14. Water-filled mesocaverns in the phreas 15. Talus, below a scar or limestone cliff.

Air-filled macrocaverns (dry caves)

The longest, biggest and, by any criteria, the best macrocaverns are those developed in limestone. The world’s longest cave is the Mammoth Cave system in Kentucky at over 540 kilometres, while the deepest is the Réseau Jean Bernard in the French Pyrenees at over 1600 m deep. Our longest cave, the Ease Gill system in Yorkshire, 70 km long, can manage only 15th place in the world ratings. The ages of caves vary considerably. Recent estimates suggest that certain limestone cave passages in North America could have formed 10 million years ago, while some tropical limestone caves are estimated to be only around 100,000 years old.

Substantial caves are not by any means confined to limestone. Other notable caves are formed by solution of marble, dolomite and non-carbonate rocks such as gypsum (e.g. Optimisticheskaja in the Ukraine, 183 km long); rock salt (in arid regions); and even quartzitic sandstone (e.g. Sima Aonda in Venezuela, 362 m deep) – while lava tubes are formed by the crusting-over and subsequent draining of molten lava flows (e.g. Kazumura Cave in Hawaii, over 20 km long). The latter include the youngest of all caves, formed on the slopes of Kilauea Volcano in Hawaii within the last five years. Other significant caves may be formed in a range of different rocks and within accumulations of large talus boulders (e.g. Lost Creek in Colorado, USA), by gravity sliding (gull caves), tectonic movements, wind-, or wave-blasting and other mechanisms. Most bizarre of all is Kitum Cave on Kenya’s Mount Elgon, which has been literally eaten for 200 m horizontally into a bed of volcanic ash by generations of salt-hungry elephants.

In caving parlance, a ‘dry cave’ is one which a human visitor can explore without getting wet. While such caves may provide an easy route into an underground world of great beauty, budding cave biologists may be greatly disappointed not to find every surface festooned with strange, eyeless arthropods, armed with sweeping antennae, stalking around on matchstick legs. As stated earlier in this chapter, dry passages in tropical caves may contain huge populations of bats or birds and a wealth of guano-associated cavernicoles, but in Britain and Ireland, cave-roosting bats and the species which depend on their presence have become increasingly scarce in recent years. Nevertheless a surprisingly large number of our macrocaverns do still harbour small populations of bats and a few associated ‘battelite’ species, which will be considered in Chapters 4 and 5.

Fig. 2.7 Mexican Free-tailed Bats, Tadarida brasiliensis, stream out of the entrance of Carlsbad Caverns at dusk. (Chris Howes)

The main biological interest of our dry caves is that they may contain the only accessible populations of cavernicoles primarily adapted to other, relatively inaccessible habitats. Thus, drip- or seepage-fed pools, gour pools and wet flowstone may harbour aquatic mesocavernicoles; and rock piles, flowstone pockets and ‘deep cave’ or ‘stagnant air’ environments may give us a rare glimpse of the terrestrial mesocavernicolous fauna.

Vadose macrocaverns (wet caves)

Cave streams may contain water derived from permanently-flowing surface streams, swallowed through an open sinkhole, or percolation water which has collected gradually from a large number of mesocavernous inputs. Those fed entirely by percolation water or seasonal run-off tend to hold more biological interest, as the populations they contain (being genetically isolated from surface habitats) may have evolved specialized features.

Surface streams arrive in the cave complete with a biota of their own, most of which will survive quite well in darkness for some considerable time, though few species may succeed in reproducing. Apart from the lack of growing green plants, and a tendency to experience less seasonal temperature change, such streams do not differ significantly as a habitat from streams above ground. The terrestrial habitat in stream passages is usually draughty and moist. Its fauna may include the adult stages of aquatic insect larvae swept in with the sinking stream, and various predators, such as spiders, which feed on them, plus a range of detritivorous cavernicoles.

Where stream passages enter the phreas (cavers’ ‘sumps’, marking the end of exploration to all but divers) it is not unusual to find accumulations of organic detritus deposited by floods. Given a suitable microclimate, such places may be well populated by specialized cavernicoles, or ‘troglobites’. Indeed, in many food-poor cave systems (such as those in mountainous areas of the Pyrenees and Cantabrians) this may be the only habitat in which cavernicoles occur in any numbers.

Water-filled macrocaverns (phreatic caves)

The chemistry, food supply and fauna of phreatic waters is determined to a large extent by their mode of entry into the cave. Underground waters are classed as autogenic (originating as through-soil percolation via diffuse seeps and subcutaneous flow) or allogenic (sinking streams). The former tend to be lower in organic content, less chemically aggressive by the time it reaches the phreas and may carry a lower sediment load. Phreatic waters may have a very different chemistry to the vadose waters which feed them, because they are unable to de-gas the carbon dioxide produced by microbial oxidation of organic materials, or to replenish oxygen used up in such decomposition.

The rate of flow in large-diameter phreatic tubes is generally greater than in phreatic mesocaverns, but is still often sluggish enough to accommodate small, slow-swimming cavernicoles (such as Niphargus fontanus), which avoid fast-moving vadose streamways.

In recent years cave divers have penetrated great distances into freshwater phreatic macrocaverns, and to considerable depths, but to date no detailed studies have been made of the biota of this remote and fascinating environment.

Water-filled mesocaverns

Most of our knowledge about the structure of mesocaverns comes from looking at exposed joints or bedding planes in limestone quarries, or occasionally caves, and from the work of karst hydrologists. We know that the very earliest stages of cave development occur under phreatic conditions, eventually creating inter-connected systems of conduits which may be in any plane, from horizontal to vertical. Phreatic mesocaverns may take the form of wiggly networks of small-diameter tubes (anastomoses), or thin, but laterally-extensive cracks, or narrow shafts – and are probably as common in other cavernous rocks, such as chalk or gypsum, as in limestone. Evidence that such spaces are inhabited comes from the animals found in well-water over the centuries. It is ironic that the earliest records of our cave fauna should be from a habitat about which little more is known today than a century-and-a-half ago, when Philip Henry Gosse wrote:

“recently, investigations in various parts of the world have revealed the curious circumstance of somewhat extensive series of animals inhabiting gloomy caves and deep wells, and perfectly deprived even of the vestiges of eyes … even in this country we possess at least four species of minute shrimps [all of which] have been obtained from pumps and wells in the southern counties of England, at a depth of thirty or forty feet from the surface of the earth.”

There is no way at present of collecting information directly about how aquatic cavernicoles use mesocavernous bedrock cracks, but it seems likely that great local variation exists within this habitat in terms of oxygen concentrations, pH and food supply. Such factors are likely to influence the distributions of the fauna, and will be discussed in Chapter 4. Fortunately there are other, more accessible types of water-filled mesocavernous habitat which are easier to study. They include the deeper interstices of stream-bed cobbles (phreatic nappes), and a peculiar sub-soil phreas of mesocavernous dimensions which occurs on the surface of impervious silt or clay deposits in mountainous areas of Europe (the hypotelminorheic medium). In both these habitats, the food supply comprises dissolved or finely particulate organic material, and the waters tend to be rather low in oxygen; and both contain faunas very similar to those of limestone mesocaverns.

Amphibious mesocaverns

As no detailed investigation of the biology of air-filled mesocavernous habitats has yet been attempted, we are forced to infer what we can about the conditions within them from studies of limestone caves and other similar habitats.

As soon as mesocaverns develop an airspace, they become available for colonization by terrestrial cavernicoles. However, cracks and anastomoses are extremely flood-prone, often filling up with water each time there is heavy rainfall at the surface. Vertical cracks probably flush more violently, but remain water-filled for shorter periods than horizontal cracks, and this may result in some differences in their faunas. Less immersion-tolerant organisms may tend to inhabit the wider, better-drained vertical cracks and humid terrestrial cave habitats, while the more aquatic organisms may prefer horizontal cracks or cave pools. It is likely that particulate organic material accumulates at specific points within the cracks (perhaps at the upstream ends of permanently flooded sections), so that some patches of habitat will be better supplied with food than others. Some areas may be too anoxic to support any life other than anaerobic micro-organisms, while some patches may harbour relatively large concentrations of detritivorous invertebrates. As previously discussed, there may be an almost complete overlap in distribution between the ‘terrestrial’ and ‘aquatic’ components of the fauna of such habitats.

The French biospeleologists Juberthie, Delay and Bouillon consider that mesocavernous spaces in fractured rock immediately below the soil constitute a habitat which is separate from caves, which they have termed the ‘Superficial Underground Compartment’ (SUC). Their claim rests on differences between the fauna found here and that found in deep caves. They consider the primary cause of such differences to be the greater temperature variation experienced in the ‘SUC’ compared with the ‘Deep Underground Compartment’ (DUC) represented by deep fissures and caves. While this may be so in SUC habitats beneath shallow soils of regions which experience a strongly seasonal temperate climate, I would doubt that the microclimate in deeply-buried SUC habitats or those of tropical karst differs a great deal from that of the ‘DUC’ – and there is evidence that cave faunas migrate up into the SUC periodically in order to exploit the resources they contain. For the purposes of this classification, I propose therefore to treat the ‘SUC’ as part and parcel of other intermittently-flooding mesocavernous spaces, whether they be immediately below the soil, within cave passages, or connecting one with the other.

There would seem to be little doubt that the SUC within calcareous rocks is by far the most extensive and important of all cave habitats in terms of the numbers and diversity of its biota. Since their ‘discovery’ of the ‘SUC’ (an environment previously well-known to karst hydrologists as the ‘subcutaneous zone’), Juberthie and Delay have gone on to show that this habitat and its biota not only occurs in limestone and other cavernous rocks, but also in ‘non-cavernous’ shales, granites, schist, gneiss, sandstones, etc. My first reaction on reading the paper announcing this discovery was to attack the bottom end of my garden with a pick and shovel. There, to my delight and amazement, I found tiny-eyed cave spiders (Porrhomma egeria) frolicking among the fractured chunks of Pennant Sandstone just one metre beneath the wreckage of the flower bed. As far as I know there has been no systematic investigation to date of the fauna of ‘SUC’ habitats in Britain and Ireland – an extraordinary gap in our knowledge which surely must be remedied before long.

A better-known mesocavernous habitat is contained in talus, or scree, whose surface can frequently become covered with vegetation and soil, turning it into a fair imitation of Juberthie and Delay’s SUC. When not sealed by soil, the upper levels of talus are unsuitable as a habitat for cavernicoles, being too cold in winter, too hot in summer and too dry for much of the time. However, if the scree is deep enough, the lower levels must surely provide exactly the conditions favoured by cavernicoles, though I know of no work on this deep-talus habitat in Britain.

I know of only two accessible ‘DUC’ mesocavernous habitats within caves. One is in the spaces within rock piles (underground talus), the other is in speleothem pockets. Rock piles may, or may not provide a suitable habitat for mesocavernicoles. If the pile is in an old, dry ‘fossil’ passage, as most rock piles tend to be, it is unlikely to contain enough food to support life (unless the cave contains bats, or other vertebrates, in which case the rocks may be over-run by guano-beasts). On the other hand, if the pile is sufficiently extensive, and is traversed by percolation water carrying organic material, it is likely to harbour a rich fauna of mesocavernicoles – although the depth within it at which a searching biologist can expect to ‘strike bugs’ will increase with the increasing dryness or breeziness of the surrounding cave atmosphere, precisely as would be the case with above-ground talus. Juberthie (1983) gives an interesting example of a schist-boulder pile in the great Salle de la Verna chamber in France’s Pierre Saint Martin cave. It is inhabited by a typical SUC fauna of Aphaenops beetles which appear to be quite oblivious of the fact that their schist scree habitat lies the best part of 1000 m underground.

Speleothem pockets are essentially just spaces of mesocavernous dimensions like all the others described in this section, but where they occur in the ‘deep cave’ or ‘stagnant air’ zone of caves (see the microclimate section, later in this chapter), they will often prove to be the very best places to look for mesocavernicoles. Speleothems occur where percolation water, rich in dissolved lime, intersects a cave passage. Where such deposits are laid down over mud, pockets often form between the two; and if deposition is still in progress, trickling water maintains just the microclimate conditions favoured by cavernicoles, while also supplying a source of food. In short, they perfectly reflect conditions in the mesocaverns. The late A. Vandel, in his famous book Biospeologie la biologie des animaux cavernicoles (published in 1964), described such a habitat in the Grotte de Sainte-Catherine, at Balaguères, in the Ariège region of France:

“One side of the chamber is formed by a stalagmitic wall which is covered by a thin layer of water which flows from an opening in the roof … The constant flow brings in organic material from the exterior which nourishes the Collembola and nematoceran Diptera on which Aphaenops (a blind cave beetle) feeds … The stalagmitic covering is separated from the wall by a space of a few millimetres which contains the products of dissolution of the rock: clotted red and black clay, and black magnesium deposits.

When one enters this chamber three or four Aphaenops can usually be seen running on the wall in search of food … If they are caught, others appear. Closer examination soon explains this phenomenon. The calcareous wall is formed of stalagmitic columns arranged parallel to each other. Between these columns small holes have been hollowed and it is into these that Aphaenops disappears … It appears that the space between the rock and the stalagmitic wall constitutes the biotope in which Aphaenops lives when not in search of food, and in which they reproduce.”

Cave pools

Gours, or rimstone pools are formed by seep-fed, lime-rich waters trickling down an incline in an open cave and depositing a sequence of curved, retaining dams. Such pools presumably provide conditions akin to those in phreatic mesocaverns, and often harbour a similar fauna, which is augmented in the cave by animals washed out from seepage cracks during heavy rain. Other drip-fed pools may also contain aquatic mesocavernicoles, providing they receive a food supply.

The concave meniscus of pool surfaces may act as a deadly trap for soil and mesocavernous springtails (see Chapter 5), providing a happy hunting-ground for other specialized mites and springtails, whose feet are equipped to grip.

Cave sediments

All kinds of sediments find their way into caves. Many arrive complete with their own specialist biotas: bacteria, fungi, nematodes, earthworms and so on, and these may be exploited by cavernicoles as a source of food. Cave sediments may also serve as a habitat for the eggs, larvae, or pupae of cavernicoles.

Moonmilk

Moonmilk is a term applied to white, wet, cheese-like or dry, sticky, powdery formless masses found in limestone caves. This weird stuff may contain a cocktail of carbonate minerals – including calcite, aragonite, monohydrocalcite, magnesite, hydromagnesite, nesquehonite and huntite – some of which are alledged to be associated with particular bacteria isolated from moonmilk. A blue-green alga Synechococcus elongatus found growing in moonmilk in complete darkness must have been using alternative metabolic pathways to the normal photosynthetic ones it employs in the light, and other algae (Gleocapsa magna) may also be present. I know of no cavernicolous animals associated with moonmilk, so this is not a habitat which I propose to discuss further in this book.

Submarine and intertidal cave habitats

The submarine Green Holes and intertidal Brown Holes of Doolin, in County Clare, are ordinary limestone caves, formed in the usual way, which became inundated by rising sea levels at the end of the last glacial period – about 12,000 BP No doubt they have had a long history of intermittent sub-aerial cave-development during cold glacial periods of low sea-stance, alternating with periods of immersion in sea-water during interglacial warm spells, such as the planet currently enjoys. They provide a significant habitat for marine life – Mermaid’s Hole has been explored for over a kilometre and the Hell complex totals several hundred metres. Other significant submarine caves occur in the Brixham area of Devon and at Durness in the far north of Scotland. Otter Hole, a resurgence cave which opens on to the banks of the river Wye near Chepstow, has a tidally-flushed entrance series which may contain fresh or saline water, depending on the height of the tide and the volume of the cave river. The faunas of such caves will be discussed in Chapter 5. In other countries, an interesting fauna has been found in coastal brackish groundwaters, but I know of no such British fauna. It may exist, but no studies have been made.

Submarine caves, such as the Green Holes, should not be confused with ‘sea caves’, such as the famous Fingal’s Cave in the Hebrides, which are spray-filled holes blasted out of cliffs by wave action. The latter may harbour a few ubiquitous, fast-moving cliff-dwellers such as sea slaters (Ligia oceanica) and silverfish (Petrobius maritimus), which can dive into cracks to escape the force of the waves, as well as a few of the more hardy marine organisms found in the more extensive drowned limestone caves referred to previously. In short, the fauna of sea caves is unremarkable.

Slutch caves

Slutch is the onomatopoeic term given by Wainwright to the peat bogs of Kinder Scout, Bleaklow and Black Hill in Derbyshire. Apparently, water flowing between the base of the peat and the underlying gritstone has carved out a number of caves of explorable dimensions – one of which has been followed for 50 m underground by cavers Steve Fowler and Tony Moult. It seems that the base of the peat is riddled with such caves and with smaller air- or waterfilled passages of mesocavernous dimensions. No doubt this will prove to be a widespread habitat in upland peat deposits throughout Britain and Ireland, perhaps with a characteristic fauna all its own, which for the moment appears to have escaped investigation.

Mines, tunnels, cellars and tombs

As artificial caves, such spaces may be inhabited or visited by any cavernicoles which have both the motive and the opportunity to do so. The motive will be a suitable medium/microclimate and food supply (see following sections). The opportunity will fall to any cavernicole whose habitat intersects the artificial cave.

Food supply

Chlorophyll and sunlight are the elements of life on earth and the source of that unique green glow which identifies our living planet when seen from space. Photosynthesis lies at the base of the food chains in which all life is meshed: fish, fowl and fungus; tree, turtle and tiger – or almost all.

In 1977, an American ship on an oceanographic survey south of the Galapagos Islands, located some active volcanic vents on the sea floor at a depth of 3 kilometres. An instrument pod was sent down, armed with video cameras to record the scene. As the probe moved towards the vents, the watching scientists were amazed to see their monitor screens fill with a writhing mass of enormous worms, 10 centimetres thick and up to three metres long. Close by were beds of 30 cm-long clams. Among them swam shoals of fish, and white crabs scuttled across the black basalt rocks. At these depths, far beyond the reach of sunlight, life is generally thin on the ground. A few starfish, crinoids and crustaceans subsist on the steady drizzle of detritus, and are in turn eaten by predatory fish. To find such an abundant local concentration of large organisms clearly pointed to an unusually rich food source. The mystery was soon solved. The volcanic vents, it seems, were spouting superheated, sulphurladen water. As this cooled, clouds of black sulphides formed and were immediately consumed by great concentrations of bacteria. The worms and the clams were feeding on these bacteria and they in turn supported the scavenging fish and crabs. The bacteria concerned are chemo-autotrophs – that is, they can harness the chemical energy in the volcanic sulphides to power their own vital processes. What is more, this whole process and the mini-ecosystem which revolves around the ‘volcanic bacteria’ is quite independent of sunlight.

Sulphur bacteria, and relatives which derive energy by reducing ferric iron compounds, are common in caves – in sediment banks as remote from solar rays as are the depths of the deepest ocean trench. The muds where they live are home to nematode worms, known bacteria-feeders, which are hunted by tiny, scurrying beetles. How many visitors, catching sight of a cave beetle, appreciate that they may be watching one of the rarest of all living phenomena – a predator sustained, at least in part, by a food chain independent of sunlight.

The energy source for cave-based chemosynthesis generally originates outside the cave, as Carboniferous Limestone itself contains very little in the way of iron and sulphur minerals. These compounds, and the bacteria which exploit them have usually been washed in as part of the cave’s sediment load. But there is at least one energy source which may originate within the fabric of the cave itself. Most limestones contain detectable amounts of organic matter, largely in the form of hydrocarbons. Such material would be of no use to animals directly, but if there are bacteria present which are capable of using it as an energy source, it could be continually liberated into the cave ecosystem at the interface between the cave and the rock, imperceptibly, as the cave is dissolved out by flowing water. Since the organic matter in the limestone will have been derived from organisms present in the seas when the rock was being laid down, its energy content must originally have come from the sun. It is in fact fossil solar energy.

Interesting though they may be as a scientific curiosity, chemo-autotrophic bacteria contribute only slightly to the food base of most cave communities. By far the biggest source of energy is still the sun’s rays, but at second-hand, in the form of introduced detritus from surface communities; for no green plants can survive in the absolute dark of the cave.

The absence of green plants in caves led early biospeleologists to the conclusion that cavernicoles are starved animals. In 1886, Packard insisted that the shortage of food available to cave animals is the reason for their small size. While it is self-evident that large animals with a high metabolic rate can have no place in an entirely heterotrophic, food-poor ecosystem, in reality many cave species are actually far larger than their surface relatives. Most recent studies have shown that cave-evolved animals (troglobites) have unusually low metabolic and growth rates and that they save energy in every way possible, by streamlining their movements and by adopting highly efficient foraging and reproductive strategies. These are obvious specializations to cope with a low food supply, and seem to be a fundamental characteristic of cavernicolous evolution at temperate latitudes like ours. Some cave species are remarkable in their metabolic efficiency and consequent ability to tolerate starvation. Gadeau de Kerville (1926) reported that a specimen of the Slovenian cave salamander, or Olm (Proteus), had been kept in captivity for fourteen and a half years, and for the last eight of these had received no food. He did not report whether it eventually died of starvation or just plain old age.

Some more recent cave biologists have noticed that captive Olms regularly slough and then eat the mucus layer which, like an extra skin, covers and protects their whole body. Mucus is sticky and microscopic examination has shown that in captive amphibians it becomes encrusted with bacteria, algae and protozoa. So de Kerville’s amazing ‘non-feeding Olm’ may all the time have been sneaking clandestine meals of diatoms-in-slime – not the tastiest of fare, but enough to keep it ticking over. Streams sinking into caves must carry with them a fair load of phytoplankton, and it may be that the Olm’s mucus-eating behaviour in captivity has some adaptive significance in the subterranean rivers where it lives.

Fig. 2.8 Olms (Proteus anguinus) – blind, depigmented cave salamanders which retain gills and an aquatic lifestyle as adults.

In a closed system, such as our Olm aquarium, the recycling of dissolved nutrients could go on endlessly, providing the Olm did not lock them up as extra Olm tissue. Once equipped with a source of energy – sunlight from the nearest window will do – the tank becomes a self-perpetuating ‘mini-ecosystem’. Because caves are perpetually dark, production cannot meet demand and they can therefore never be considered as proper self-sustaining ecosystems. But the waters which form, enlarge, infill and eventually destroy caves almost invariably carry organic compounds – complex chemicals gathered from the soil or the breakdown of animal and plant detritus. Organic chemicals (dissolved in water, or clumped together in big lumps of detritus) fill the role of an energy source in the cave. There has been much speculation by cave biologists over the extent to which dissolved organic substances can be absorbed directly by aquatic cavernicoles. So far the evidence is inconclusive, but there is no doubt that they are captured by microfungi, bacteria and protozoa, which are plentiful at least in some allogenic cave waters. So, one way or another, all organic material entering the cave becomes available to the bottom rung of cave animals – the detritivores which fill the equivalent role to the primary consumers of the sunlit world above.

While the photosynthesising parts of plants have no place in caves, there is no reason why their roots should not penetrate into subterranean voids. Indeed, in the lava tubes which run just beneath the skin of the active volcanoes of Hawaii, tree roots form dense subterranean forests which support a range of sap-sucking bugs, root-chewing caterpillars and their predators; pale-skinned, eyeless relatives of species found in the forest above. Roots seldom penetrate into macrocaverns in Britain, but they may constitute a significant food source in a number of other cave habitats, such as the SUC, culverts and slutch caves. No one seems to have investigated root-associated faunas in such locations, but it would surprise me if such a widespread niche is not occupied by at least one insect specialist.

Second-hand plant material takes many forms: autumn leaves carried on a sinking stream, tree trunks hurled into a pothole by violent floods, or well-rotted humus quietly inched down the cracks of a limestone pavement. Usually by the time such materials reach the depths of the cave where the true cave faunas live, they have been thoroughly pulverised by water and rock, tenderised by bacteria and fungi, and often enough, passed through a series of invertebrate guts.

This was brought home to me during my first visit into the higher levels of GB Cave in the Mendip Hills, several years ago. The upper levels of the cave contain a series of narrow rifts which leak water from the overlying land whenever it rains. I was hunting for tiny cave beasts in these upper levels, and looking out for patches of fresh mud which I guessed would be organically richer and so would contain more life. I soon began to realize that each and every sediment cone emanating from each and every leaky crack was made up of thousands of tiny mud pellets, like scaled-down grains of rice. They were arthropod droppings – hundreds of millions of them, forming a deposit which over the centuries was gradually filling up the upper dry passages, and probably the lower reaches beneath the water table too. Fortunately, most cavers are blissfully unaware of the true nature of the substance which they spend each weekend crawling through and, no doubt, liberally ingesting themselves.

Biologists used to studying ecosystems based on living plants too often treat detritivores – animals which eat dead organic material – as a single dietary category. In the cave ecosystem, all the first-level consumers are ‘detritivores’ and it is surprising just how many different specializations they manage. This is most clearly seen in guano communities, where chains of very specialized organisms use different components of the insect remains which form the bulk of bat droppings. Stuart Hill has studied the ecology of one such community in a bat cave in Trinidad. Guano of the funnel-eared bat, Natalus tumidirostris (notorious, incidentally, as a carrier of the human diseases, relapsing fever and blastomycosis), was eaten as soon as it fell by a cockroach, Eublabarus distanti, which removed most of its fat and some of its protein (much of the unbound protein having been already stripped out in the gut of the bat). The cockroach droppings, still rich in chitin, were decomposed by a fungus, Penicillium janthinellum. This in turn was fed on by the mite Rostrozetes foveolatus and various other tiny arthropods. The mites in turn were eaten by other arachnid predators. Similar sorts of food chains probably operate in British bat caves, but the research has not yet been done.

In our present ignorance, we really do not know exactly what many of our British cave detritivores get out of their ‘junk food’ diets. There must be some degree of specialization, because certain types of materials are largely ignored by certain cave animals, while others attract them strongly.

One way to study dietary specialization is to put down baits in the cave and see what species come to them. The baits should be very small or they will provide an un-natural boost to the numbers of certain species and so upset the balance of the cave community.

I tried a baiting programme in the Ogof Ffynnon Ddu system in Wales, during the course of a wider survey of the fauna. I already knew, from a number of earlier collecting visits, that at least six species of fly were common in the upper level passages (a dung fly, a coffin fly, a winter gnat, and three or more fungus gnats), together with eleven springtail species, a millipede, a woodlouse and various beetles and mites. All were associated with detritus in one form or another, so when I put down small pieces of raw liver or cheese in various choice spots, I expected to gather quite a collection of invertebrates. Over the next couple of weeks I came back regularly to check the baits and was disappointed to find nothing on them. By now the liver was beginning to get a bit unsavoury and the cheese had gone slimy. Two and a half weeks after placement, I found every single liver and cheese bait crawling with the slender maggots of the winter gnat, Trichocera maculipennis, but still nothing else came near them. Eventually, the larvae crawled away to pupate, the bacterial smell subsided, and only then did a few Folsomia springtails gather in the area. So, far from being unspecialised scavengers, these detritivores showed themselves to be quite a discerning bunch.

One of the key factors in determining how the cave fauna will respond to a particular source of detritus seems to be whether it is first attacked by fungi or bacteria. Many fungi exclude bacteria from their chosen food by secreting antibiotics, and avoid other foods of the wrong pH which are decomposed by bacteria. Sometimes the dominance of either one or the other is determined by the size of the potential food source. In the course of a study of lava cave invertebrates on Kilauea volcano in Hawaii, I put out baits of supermarket white bread, to see what would be attracted. Some baits were in the form of crumbs spread along the rough cave wall, others were big chunks which I kneaded into golf-ball-sized lumps. The crumbs quickly went soggy and grew a thin gelatinous slime of yeast-like fungi which attracted cave-specialised millipedes and crickets; while the chunks became bacterial stink bombs infested by scuttle-fly maggots, but shunned by all the true cave fauna.

Several European biospeleologists have noticed a similar specialization between bacterial- and fungal-feeders. In general it seems that ‘surface grazing’ arthropods, such as millipedes, isopods and springtails, tend to be fungus-eaters; while ‘gulpers’ and burrowers, such as fly larvae and earthworms tend to be bacterial feeders. However, even closely related species within the same group can specialize to different foods to avoid competition. An example is found in the springtails Tomocerus minor and its congener T. problematicus, which co-exist in similar habitats in the Grotte de Sainte-Catherine, in the Ariège region of France. The former mainly munches fungi, while the latter feeds largely on bacteria-rich silt.

In general it seems that microfungi, which occur on a variety of substrates, including wood, animal faeces and plant detritus, form the most important dietary component for most terrestrial cavernicoles. In a study of several Virginia caves, Dickson and Kirk (1976) found that the abundance of the cavernicolous invertebrates was correlated with the abundance of microfungi and with high fungal-bacterial ratios, but not with abundance of bacteria or actinomycetes.

Friedrich, Smart and Hobbs (1982) summarized the literature on bacterial counts for cave sediments and waters. As might be expected, heterotrophic bacteria (which feed on inwashed organic material) are far more numerous than autotrophic bacteria (which utilise the oxidation of inorganic compounds) – but there are very wide variations. Sediments give consistently higher bacterial counts, generally of the order of 10 x 10⁶ g⁻¹, but with large variations either side; while cave waters give very much lower counts, generally of the order of 100 ml⁻¹. These authors’ own figures for different types of water inputs in Mendip caves are interesting. Swallets feeding directly into open cave passages give the highest figures (500 ml⁻¹). Percolation recharge which is integrated into mesocavernous fissures and conduits has an intermediate bacterial count (50–300 ml⁻¹), while diffuse flow waters in phreatic microcaverns (sampled via boreholes) give a very low count (2 ml⁻¹). One of their conclusions is that water flow through the limestone aquifers feeding the major springs used as drinking supplies around Mendip does not provide any significant filtration of microbial input. While bacterial counts at the major Mendip risings in general do not give cause for public health concern, this may not be the case in other springs, particularly in tropical countries, used as an untreated drinking supply on the supposition that water which bubbles out of the ground must be pure. Sinkholes are widely used as rubbish dumps, attracting disease-carrying rodents, and the water which enters them may reappear many miles away as a spring, perhaps in a different valley. The late Dr Oliver Lloyd, a well-known Mendip caver, contracted Weil’s Disease from Leptospira bacteria present in Longwood Cave on Mendip, while several members of expeditions to Borneo in 1980 and 1984 (myself included) contracted a similar form of leptospirosis in the famous Mulu caves, and nearly died as a result.

In slow-moving underground streams with mud bottoms, and in drip- and seep-fed pools isolated from swallet-fed streamways, microfungi are more common than bacteria and are correlated with the abundance of macroscopic cavernicoles. Microfungi and bacteria may be utilized directly by such cavernicoles, or may be eaten by Protozoa, nematodes and other micro-fauna which are in turn eaten by Crustacea (isopods and amphipods) and aquatic insect larvae.

I have tried so far to paint a picture of the cave community as a fairly structured world, where, despite the absence of green plants, the lowly animals at the bottom of the food chain still manage a fair degree of dietary specialisation, preferring some kinds of detritus or living prey over others. In fact, the degree of specialization may be even more pronounced: not just according to the nature of the food source, but even according to the size chunks in which it is packaged. Thomas Poulson and Tom Kane, working in the enormously complex Mammoth Cave system in Kentucky, have found that the terrestrial arthropods in the cave use energy availability as the main basis for dietary specialization. Of the 44 species regularly recorded in their study area, 30 were primarily associated with one food, seven with two, six with three, and two with four of the six natural foods available to them. All the species which used more than one food source picked different stages in the decomposition of each of their foods, or different places along the gradient of food concentration so that they fed at a unique level of energy availability. Two millipedes illustrate how this works. Scototerpes feeds on the scattered droppings of cave crickets and to a lesser extent on very dispersed leaf litter in the last stages of decomposition and on veneers of leached organic matter deposited by floods on the cave ceiling and walls. The other common cave millipede, Antriadesmus specializes on cricket droppings in areas where they form thick deposits. Not surprisingly, the latter species turns out to have a higher metabolic rate and to lay more eggs than its more frugal cousin.

Poulson and Kane’s finding may go some way to explaining the unattractiveness of my cheese and liver baits in OFD. It could be that unusual concentrations of protein-rich food entering an oligotrophic (food-poor) cave, may be shunned by the cave community (except guanobia) as they represent a level of energy availability well above that to which the cavernicoles are adapted. But there may be a simpler explanation. Kathleen Lavoie of the University of Illinois noted that certain cave fungi grew better on large droppings (such as those of pack rats) than on those of smaller species. Rapid colonization by fungal hyphae formed a meshwork barrier which seemed to exclude cave arthropods from this otherwise tasty food resource. So, far from cave arthropods shunning large items of food, it may be that other, more opportunistic forms of life actively keep them at bay.

So far, we have considered only detritus as a food-source. While in sheer numbers, detritus-eaters must of course form the bulk of the cave community, it is predators and omnivores which have the greatest scope for dietary specialization, providing they are able to survive at low population densities. The predators in British caves are unspectacular creatures: mites, spiders, beetles and their larvae, amphipods, caddis larvae and flatworms. Once again, we can only speculate as to the degree of ecological specialization which they enjoy – they have not yet received any detailed study in Britain. The Americans, however, have studied their own equivalent species in considerable detail and, as there is no reason to expect cave predators of temperate American caves to behave very differently from our own, their research findings are worth repeating here.

Tom Barr studied six cave-evolved ground beetles which co-exist in Mammoth Cave. One of them, Neaphaenops tellkampfi, feeds almost exclusively on the eggs of cave crickets. It finds them by smell, digs them out of the sand in which they were laid, then punctures them with specially-elongated mandibles and sucks out the contents. The other five beetles are all closely related in the genus Pseudanophthalmus, and all feed on different prey or in different microhabitats. Even the two near-identical-looking species P. menetriesii and P. striatus feed quite differently: one hunts for small arthropods in rotting wood, the other digs for tubificid worms in cave silt. Our own cavernicolous carabid, Trechus micros, feeds in a similar way. I have watched it work over a tidal mud bank in Otter Hole in the forest of Dean, pocking the surface with hundreds of tiny pits, as it thrust its head repeatedly into the soft sediment in search of prey.

The tidal mud of Otter Hole is an unusual cave sediment which supports an exceptional fauna. Estuarine muds of the Bristol Channel have been estimated to have a productivity four times that of good arable soil. They are rich in organic material and correspondingly smelly. The mud is kept sloshing up and down the upper reaches of the estuary by fierce tides which have an amplitude here of 13 m, one of the greatest tidal ranges anywhere on our side of the Atlantic. During the highest Spring tides, when the cave stream is itself swollen by rains, it is usual for the entrance passages of the cave to flood right up to the roof and to stay flooded for several weeks. Cavers know this, and avoid the cave during this danger period. Eventually the trapped waters drain slowly away, but in the meantime their sediment load has settled out as a rich brown deposit which coats the walls and ceiling of the cave right up to the high-tide mark. The new mud is soon invaded by a wealth of invertebrates, including a millipede, Brachychaetuma melanops, and a rove beetle, Aloconota subgrandis, found in no other British caves. The richness of the cave fauna is a direct result of the floods.

The importance of seasonal flooding to cave invertebrates has been noted by many biospeleologists. In the food-poor alpine caves of the Pyrenees and Spanish Cantabrians, almost the whole fauna lives in the ‘intertidal zone’ of flood-prone passages. In the enclosed space of a cave, flooding can take one of two forms: ‘flash floods’ and ‘ponding’. In the former, a sudden rush of water temporarily approaches the carrying capacity of a streamway, sweeping all before it. This is the type of flood dreaded by cavers, and passages which are prone to such events are rigorously avoided whenever there is a risk of heavy rain in the catchment area. ‘Ponding’ floods happen more gently. They usually occur where collapsed blocks or sediment impede the flow of escaping water, so that any slight increase of input causes a temporary pond or lake to form behind the obstruction. The water may have been flowing quite quickly up to the barrier, but now it slows, depositing its sediment load. As the waters recede, the local invertebrates rush out of hiding to ‘beachcomb’ for the juciest morsels.

In temperate caves, flooding is a strongly seasonal, and therefore predictable, phenomenon – and many cave species time their cycles of activity and reproduction around it. The advantage of synchronized breeding is obvious in cave species which occur at low densities and in which only a small proportion of females are capable of reproduction in a given year. Tom Poulson, of Yale University, has made a special study of aquatic cave communities in the USA. He explains the complex relationship between cavernicoles and floods as follows:

Fig. 2.9 The ground beetle Trechus micros digging an enchytraeid worm from the silt of Otter Hole in the Wye Valley.

“Annual growth and breeding cycles in caves are cued by spring floods, specifically by changes in temperature, food supply, amounts of solute, turbidity and current … Scale growth rings of amblyopsid cave fish, and probably other cave fish, form during floods while plankton and organic matter are being replenished, but the fish are secretive, inactive and not feeding. The amblyopsid cave fish Chologaster agassizi, Typhlichthys, Amblyopsis spelaea and A. rosae breed in spring towards the end of the yearly floods or high water, and the young appear during the period of low water 3 to 8 months later when residual food is still present and chances of injury from floods are low. … Some snails, isopods, amphipods and decapods also breed in spring and early summer … [for example] breeding in the shrimp Paleomonetes ganteri and the crayfish Orconectes pellucidus precedes high water, with maximum organic inwash, by 4 to 6 months.”

James Keith has found a clear seasonal reproductive cycle in the American cave beetle Pseudanophthalmus tenuis, which inhabits flood-prone mud banks in Murray Spring Cave, Indiana. Across the Pacific, Chris Pugsley has studied the New Zealand glow-worm Arachnocampa luminosa whose starry displays form the centre-piece of a tourist development at the famous Glow-worm Grotto at Waitomo. Although most stages are present throughout the year, numbers of larvae (the feeding stage) show a clear peak in late spring / early summer, when their food (winged imagines of aquatic insect larvae) are abundant, and the evaporation rate in the cave is at its lowest level.

Seasonal variations in food supply in caves are not due solely to flooding. Bats have a predictable seasonal occurence in temperate caves, and this might be expected to strongly affect members of the guano communities which depend on their presence. Harris (1970) has described the cycle associated with occupation of a cave by a maternity colony of Bent-winged Bats in Australia. As the bats arrive, there are fast changes in food, temperature, moisture relations and pH. Food quantity, rate of daily input and freshness all increase. The guano temperature rises 10°C within a week. The fresh guano, along with bat urination combine to increase the relative humidity from 60 to 95%, and the substrate becomes visibly moist. The urine-ammonia aerosols and faecal material modify the substrate pH and other chemical characteristics. How guanobious cavernicoles respond to such changes does not seem to have been studied in any detail, but it is known that population levels of many species of guanobia increase sharply when fresh guano becomes available, and decrease when it is not.

Microclimate

Until a few years ago, I had often wondered how the ‘terrestrial’ inhabitants of flood-prone passages and mesocavern cracks survived the regular immersions on which their livelihoods depend. It took a visit to the New Guinea highlands to reveal the secret. I was involved, with a large British expedition, in exploring the huge labyrinth of Selminum Tem – then the longest cave in the southern hemisphere. One day, while a small group of us were in the bowels of the system, the heavens opened and 10 cm of rain fell in a couple of hours. The cave streams rose by several feet in a matter of minutes, and we were lucky to get out in one piece. Two of the team were working in a young, immature network of passages deep below the main trunk of the cave and in their haste to escape the rising water, they dropped a quantity of expensive equipment. So a couple of days later, a colleague and I returned to retrieve it. The passage had obviously flooded to the roof, and the water level was still falling, amid distant gloops and gurgles. The walls and ceiling of the passage were coated with a thin layer of wet black mud, spangled here and there with fragments of soggy biscuit, washed from a packet dropped by the fleeing cavers two days previously. Several of the fragments had already attracted beetles and millipedes, and as I watched, a glistening wet millipede slowly emerged from the depths of a crack and headed across the mud in the direction of the nearest biscuit fragment. Further along the passage, millipedes of two different species appeared to be feeding on the floor of a temporary puddle – underwater. Later I watched a woodlouse doing the same thing. It seemed that the cave community here was quite amphibious; sheltering in cracks and crevices as the waters swept through their home and sallying forth to feed once the flood had passed by.

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