Introduction

        Cercopithecus subterraneus, also known as the bluetail monkey or bluetail guenon, has the distinction of being the world's only burrowing primate.  The species was named by its discoverer, Sir Rodney Billingham-Applegate, in 1946, when he saw what he identified as an adult male diving into its burrow in the ground.  Almost a decade earlier, while completing a census of the diurnal primates of the Umbugwe Forest, he had been startled by the sudden appearance of an individual of a previously unknown species of guenon from a hole next to the lawn chair in which he was relaxing, and he spent the next eight years in a lonely and often frustrating search, enduring the frequently sarcastic disbelief of co-workers and detractors alike, before once again seeing the characteristic white chin tufts that have since become so well known and that are one of the morphological hallmarks of this shy and secretive anthropoid (Billingham-Applegate, 1946).
       In the spring of 1952, a pair of youthful primatologists from Iceland was abandoned by their guide in a practical joke and lost up the little-known Ivindo River for three and a half days, after which they emerged from the forest, blinking in the hot equatorial sun, festooned with lianas and filled with lurid and unbelievable tales of their escapades among backward native tribes and colorful spitting monkeys that lived underground (Englanberg and Petersen, 1953).  It was soon realized that these were the selfsame animals that Billingham-Applegate had identified before. The Scandinavian Primate Association lifted its suspension of the daring duo, and word quickly spread throughout the primatological establishment about this new and peculiar species of guenon.  Claims and counterclaims were penned furiously and fired back and forth, lighting up the dark pages of even such a staid and musty periodical as the British Royal Museum Journal of the Cercopithecinae
       Expeditions were sponsored and studies funded by the Margaret Mead Society of Upper Baltimore, the L.S.B. Leakey Foundation, and the Institute for Advanced and Theoretical Anthropoid Ethology in Berne, Switzerland. From 1956 to 1958, a crack team of top researchers from the Los Angeles County Museum of Unnatural History scoured the Gabonese vine forests where C. subterraneus was said to be hiding, in a fruitless and finally unsuccessful attempt to locate so much as a feces sample or a burrow entrance, and was eventually found to be in the wrong country.
       The year 1964 was marked by the publication of two books significant for their effect on the field of primate behavior.  The first was The Year of the Gorilla by George Schaller, and it was destined to become a classic of the literature. The second was The Week of the Bluetail by Delores McKenzie Waters, an account of her all too brief sojourn in Gabon, and its fate was regrettably but deservedly to languish in the dimmest recesses and most remote nooks of a few eclectic bookshops.  It was regrettable chiefly because, even if she had not been accused of outright plagiarism (she had worked for several months as one of Schaller's assistants), the book should have served as a blazing example of exactly how not to conduct such a research project.  As a direct result of the publication of this book, Dr. Waters was fired from her position on the faculty of Abodeely Junior College, the president of which declared hotly that she was the most incompetent researcher ever to follow a monkey in the wild.  Despite the fact that she returned to the field the following year, she was never able to document the interbirth interval of C. subterraneus, which was her stated goal, because she never witnessed any births, nor any mating behavior, nor indeed any social contact whatsoever, and was on only rare occasions able to spot anything at all due to her extreme nearsightedness.  The only data she managed to collect in Gabon was the actual length of time she was there, and even that was uncertain
       Five years later, the eminent Japanese primate behavioralist Professor Mitsuo Ohhohoho, flushed with success after having lived with a troop of brushy macaques for five years, began his long-term study of C. subterraneus subterraneus, the subspecies that inhabits the cloud forests of the fault-ridden Makanza Mountains.  Unfortunately, he has not yet returned, and nobody knows anything at all about his whereabouts.  In 1973, one of his proteges, Dr. Bonzai Nataka, went to Gabon to find Professor Ohhohoho, but has been unsuccessful to date.  He was incidentally also interested in investigating bluetail relations with other sympatric primates, but eventually concluded that they had none, contracted a baker's dozen of tropical diseases, and left (Nataka, 1975).
       In 1970, the feminist New Age primate specialist Maxine Williker-Rogers set out to prove that adult females in C. subterraneus exhibit a marked degree of dominance over adult males.  She discovered that the only dominance most bluetail females demonstrated was over her, and she was often displaced from her sleeping quarters by mobs of angry females (Williker-Rogers, 1972, 1973).
       Populations of bluetails have since been reported not only in Gabon, but also at Kibale Forest in Uganda (C. subterraneus maxwellii), Aberdares in Kenya (C.s. kenyaensis), Adiopodoume in the Ivory Coast (C.s.grewei), and in North Africa, although the taxonomic position and morphological affinities of the last remain in dispute, and show this animal to be better placed in Macaca sylvana.

The study

        Observations of bluetail burrowing behavior were made between June 1967 and February 1985 at the 17 sq. mile Makokou Study Area in the Ivindo River Forest Reserve which is part of Jambili National Park located in the Makanza Mountains of northeastern Gabon.  Details of this study are available elsewhere (Boué, 1978, 1979a, 1979b, 1981, Boué and Maudlin-Jones, 1983).  Unlike other guenons and indeed most monkeys and apes, C. subterraneus is predominantly solitary; adult males live alone while females are accompanied only by dependent young.  In this regard, the anthropoid closest to this social pattern would be the orangutan.
       During nineteen years, observations on wild bluetails totalled 8,620 hours.  Observations on target adult males, who are the most difficult to follow because of their nasty spitting behavior, totalled 980 hours and 15 minutes (11.4% of total observation time).  Observations on target females totalled 4,325 hours (50.2% of total observation time), and observations on independent sub-adults of both sexes totalled 3,314 hours and 45 minutes (38.4% of total observation time).
       All focal animals nested in burrows at night except for one aged female with arthritic fingers who slept in a large stone jar normally used to store grain.  Three adult males, "Micky," "Felix Frankfurter," and "Blackeye," spent more than 60% of daylight hours in their burrows, coming out only in the early morning and the late afternoon when no other bluetails were within auditory or visual range.  We found that bluetail burrows were on average 1,238 feet apart, the closest being two adult females who burrowed typically about 200 feet from each other.  Another male, "Bulu," spent an increasing amount of time in his burrow over several years, and was eventually discovered by a native child from a nearby village who entered his burrow to be deceased.
       Biogeographic zones at Makokou include primary lowland rain forest, flooded or swamp forest, riverine forest and secondary forest, all of which are inhabited more or less by the cercopithecines cephus, neglectus, pogonias, and nictitans.  In addition, there are regions of montane and bamboo forest which contain remnant populations of neglectus (DeBrazza's guenon).  Although bluetails sometimes range through these areas, they seem to prefer the relatively infrequent patches of upland vine forest for their burrows, because the pungent odor of the ubiquitous Iboúnzi vine discourages residence by other primates.  This vine is in fact so disagreeable that many observers have been forced to wear nose plugs in order to traverse the tangled terrain of these densely-forested regions.

Burrow construction

       Burrow construction at the Makokou Study Area was observed on 197 occasions.  Adult males dug 45 burrows (22.8% of total), adult females dug 98 burrows (49.7% of total), and independent sub-adults dug 54 burrows (27.5% of total).  Sub-adults began digging their own burrows at approximately three years old for males and three and a half years old for females.  Before the onset of independent burrow construction, all juveniles shared their mother's burrow.  The fact that males dug 22.8% of the total number of burrows that were observed being constructed while only accounting for 11.4% of total observation time is explicable by the slightly shorter periods they remained in each burrow before abandoning it, and by the female adults' reticence at digging burrows while someone was watching them.  Females and sub-adults dug new burrows on average roughly once a week, while adult males dug new burrows every 5-6 days.  Samples of earth and nesting material from recently abandoned burrows contained large quantities of fecal parasites of a species that incubates in 8-10 days, therefore it is assumed that bluetails leave their burrows before they can be reinfected by these parasites (Jernigan, 1982).
       Cercopithecus subterraneus exhibits little body size dimorphism between the sexes, and their burrows are of approximately the same dimensions.  Figure 1 shows the entrance to a typical bluetail burrow.  Juveniles do not have

Frequency and duration of burrowing

        Bluetail burrowing frequency varies seasonally, but not at all times of the year.  C. subterraneus spends most of its time underground.  As might be expected, adult males are the most adventurous, and can often be seen peeking bravely out of their burrow entrances.  During times of vegetational abundance, males spend an average of three and a half hours a day foraging quietly for the young leaves of several low-growing forest shrubs, and supplement their diets at other times with insects, grubs and rotting bark.  Females are more cautious and usually more sedentary, commonly remaining in their burrows until ten or eleven AM and returning to them shortly after noon, unless they are digging a new burrow.
       Table 1 shows the mean burrow time for the different age and sex classes.  These figures are subject to a substantial degree of error as a result of the difficulty of telling males and females apart.  This table does not include time spent on excavation.

Adult males
Adult females
Sub-adult males
Sub-adult females

Burrowing as an adaptive behavior

        Adaptive behaviors are those that permit the animal to adapt, and thus better to survive and/or reproduce. Therefore, in order for it to be shown that burrowing is adaptive, two things must be demonstrated:  first, that individuals must vary in the degree to which they carry on this behavior, and second, that these variances must correlate in some way to success in surviving and reproducing.   To put it simply, the advantages of burrowing must outweigh the disadvantages.
       One of the obvious disadvantages of burrowing is that it exposes the bluetail to all the terrestrial predators that inhabit the Gabonese vine forests, such as the so-called 'barber pole' python, the great white-footed mountain gopher, various badgers, and the deermouse deer, all of which can go into holes in the ground.  The bluetail has very little protection from any of these hungry hunters, except sometimes a plug of dank and smelly humous, which it will try to pull down into the burrow after it to block the entrance.  On the other hand, C. subterraneus is very well-protected from the monkey hawk, which preys on all arboreal species of guenons.
       Another obvious disadvantage, which life in the branches avoids, is that for several months every year during the rainy season, bluetail burrows are partially filled with water.  Not only does this make it more difficult to forage for food, but because of it, the bluetails must spend an hour or so every time they emerge from their burrows just drying out.  It is a pathetic scene, one which we were only too fortunate to see played out innumerable times, as the weather worsened and the wind whistled through the vines, and the bedraggled forms of unhappy bluetails began rising dispiritedly from their sodden holes.  However, during these periods, they were seldom thirsty.
       A less obvious but even more significant disadvantage of this sub-terrestrial lifestyle is that spending so much time in the dark has apparently had a deleterious effect on their eyes, and it can take them up to an hour before they are able to adjust to even the subdued light of the vine forest.  They are often seen standing beside their burrow entrances blinking rapidly, or 'eye-fluttering' as Williker-Rogers has termed it (Williker-Rogers, 1972).  At this point they are even more vulnerable to predation than usual, and coupled with the time spent drying out, and the time spent being alert for danger, and the time spent actually constructing their burrows and stealing the lining materials and foraging for food, this even further reduces the time they can spend socializing.  In fact, just how adult bluetails "get together" is still something of a mystery.  One of our native guides, Albert Mbigou, climbed down into the burrow of a female we named "Henrietta" who had not emerged during the daytime for several months, and found that she had excavated several large chambers and had dug tunnels from her burrow to the burrows of the several closest males. What was going on he could only guess at.
       The major and perhaps only discernable advantage of living on or below the ground, it would then seem, is the colonization of a niche which is at the very least underutilized by other primates (perhaps with good reason), including nesting and travel space, and food sources of presumably sufficient nutrition to meet their energetic requirements.  It can be easily seen that bluetails are perhaps the least active of all primate species, oftentimes while underground being in a state of near-torpor, and thus their energetic needs would seem to be quite small.
       Since all age and sex classes exhibit approximately the same burrowing frequency, no selective advantage would be conferred on any particular individual, either male or female.  Burrowing does not seem to be an advantageous behavior for survival (see Cooper and Somers, 1983, for a discussion of the relative longvity of different guenons, in which it is shown that bluetail longevity is 42% less than other cercopithecines with comparable body sizes and weights).  Neither does burrowing appear to be advantageous for reproduction.  Bayswater found a 16% greater infant mortality rate in C. subterraneus when compared to the mean IMR for all other sympatric primate species. Furthermore, Anderson and Richards, who studied the bluetail guenons of the Kibale Forest in Uganda, found that their burrowing rates were 32% less than the Makokou subspecies, the reproductive rate was 24% higher than the Makokou population, and the mean IMR was 41% less (Anderson and Richards, 1992).
       In light of the above factors, we cannot conclude that burrowing is an adaptive behavior, and we feel that anyone who does is loony.

Burrowing as a pathologic behavior

        If burrowing can not be shown to be an adaptive behavior, should we not then think of it as pathologic?  This is the theory put forward last year by Teddy Preston and Frank Keith at the Primates Symposium held at Bob Jones University in South Carolina, and it is one to which we confess to being strongly drawn. For one thing, the total biomass of primates at Makokou is obviously much less than at Kibale in Uganda or at Kuala Lompat in Malaysia, while the available food sources are approximately equivalent (Boslington, 1983; Billabong, 1985; Preston and Keith, 1986).  The carrying capacity of the arboreal environment has thus not been reached, and there is no doubt that there are several niches that could be better utilized first without resorting to the dire expediency of going underground.
       Preston and Keith have suggested that burrowing should be viewed as one of an entire suite of behaviors, all of which stem from an obsessive and pathological fear of the forest and everything in it.  The bluetails of Makokou habitually run away from each other, they hide virtually all the time, and they use silent scent communication like the prosimians rather than loud vocalizations like the other guenons, vocalizations it should be pointed out which would draw unwelcome attention to them.  They seem to be frightened by almost any noise in the forest (see Table 2).

Things which most commonly frighten
C. subterraneus

Claps of thunder
Trees falling
Tree branches falling
Twigs and leaves falling
Trees creaking in the wind
Wind
Bird calls
Swarming insects
Solitary insects
Planes going overhead
Drilling at miners' camp 10 km away
Movements of other monkeys
Sounds of something approaching
Observer noises
Rain hitting canopy
Other

Percentage of total
frightening occurrences

1.2
8.2
7.9
4.6
7.2
3.1
17.1
10.2
8.7
2.2
3.7
14.2
2.3
7.1
1.7
 0.6

Conclusion

        Nineteen years was unfortunately not a sufficient length of time to determine whether bluetail burrowing behavior is adaptive or pathologic.  Although this activity could not be shown to be adaptive, there may be some selective advantages that we are as yet unaware of, and that we may have been unable to discern.  However, the evidence for its being a pathologic behavior based on extreme fearfulness is mounting.  We are returning to Gabon next month for the second phase of our study, and we very much hope to have a definitive answer before long.

Acknowledgements

        The guenon research on which this paper is based was funded by the Woodrow Wilson Old World Monkey
Center, the Foundation for Central African Tropical Forest Studies, Georgia Pacific Gabon, the Women's League of Ottawa, the National Science Foundation, the Harvard University Primate Center, the Ralph A. Bennett Teasdale Corporation, the Whittier Junior High School Anthropology Club, the United Nations Simian Rescue Society, the World Wildlife Fund, and the Governments of Gabon and Mali.  We are very grateful to these organizations and to the people associated with them for making this work possible.  L.S.B. Leakey's initial support was instrumental in permitting us to begin this research, and we remember him fondly.  We thank Mr. Wülü Ibouê, Director of the Makokou Study Area, and his staff for their many kindnesses and unfailing courtesy and assistance.  The Gabon Institute of Sciences and the National Forestry Service provided much help and served as our sponsors in Gabon. We express our deep gratitude to Dr. N'Bana Bongo, Dr. Trevor Umpazi, Dr. Kadroué In, Dr. Oyem Ndjole, Mr. Bitam Boouè, Mrs. Koula Okandja, Mr. and Mrs. Ayina Mekambo, Dr. Nyanga Offoué, Dr. and Mrs. Ndende Mba, Mr. Mayumba Fougamou, and Dr. Abanga Moutouuu.  Thanks also to Dr. R. Franklin Boslington and Mr. Arthur Barrett Masters.  Finally, we want to express special thanks to our local staff, Mr. Ngounie Onångue, Mr. Albert Mbigou and Mr. Lebamba Ojouab.

Anderson, Philander P. and Richards, Michael Sorenson  (1975).  "The Bluetails of Kibale."  Ugandan Forest Weekly,  1:1.

Atherington, Arthur A.  (1981).  "Morphological adaptations of bluetail guenons."  Afr. Stud. Monogr.,  12:75-91.

Bayswater, Arthur Presley  (1975).  "Infant mortality rates in C. subterraneus, C. nictitans, C. cephus, C. pogonias, C. mitis, C. campbellii, and C. ascanius.  In Predation on Primates in the Pleistocene  (ed. Parker L. Quiddy).  New York,  Jay Press.

Billibong, Matilda T.  (1985).  "Bluetails: Just How Blooming Big Are These Little Buggers?"  Australian-Samoan Nature Journal,  82:12-20.

Billingham-Applegate, Rodney  (1946).  "How I Discovered a New Species of Monkey whilst Relaxing in the Forest and Enjoying a Mint Julep."   Arch. Brit. Explor. Soc.,  212:56-81.

Bongo, N'Bana  (1980).  "Description and analysis of the head-dipping display in the Gabonese bluetail."  Rain Forest Notes,  22:41-58.

Boslington, Franklin R.  (1982).  "Vegetational zones of the Ivindo River Forest Reserve."  Biotropica,  14:50-110.

Boslington, Franklin R.  (1983).  "Biomass parameters for several endangered rain forest refugia."  Nature,  310:88-131.

Boué, Oondóué M.  (1978).  "Water retention characteristics of Gabonese montane forest soils."  J. West African Trop. Soc.,  56:22-39.

Boué, Oondóué M.  (1979a).  "Foraging strategies of bluetail monkeys at the Makokou Study Area, Gabon." Primates,  20:79-94.

Boué, Oondóué M.  (1979b).  "Seasonal variation in day-range distance of Cercopithecus subterraneus." Primates, 20:185-210.

Boué, Oondóué M.  (1981).  "Spitting proclivities of adult male bluetail guenons in the Ivindo River Forest Reserve of Gabon."  Int. J. Primat.,  2:112-186.

Boué, Oondóué M.  (1986).  "Stomach deflation as a defensive tactic in adult C. subterraneus at Makokou." Proc. Gabon Nature Soc.,  273:120-140.

Boué, Oondóué M. and Maudlin-Jones, Reginald Pennyworth  (1983).  "Bluetail monkey burrowing behavior as a possible model for early Bantu cave construction."  J. Human Evol.,  12:125-163.

Cooper, Felicia and Somers, E.B.  (1983).  "DNA chromatization tests and cercopithecine longevity."  Int. J. Primat.,  4:72-92.

Delaney, Lilian and MacArthur, Alice  (1975).  "C. subterraneus: a case of sociobiological paranoia."  Contrib. Primat.,  5:27-41.

Englanberg, Leif and Petersen, Olaf  (1953).  Two Came Back.  Reykjavik, Viking Press.

Fleiglehaus, Eric Scotmeister  (1978).  "Going down a monkey hole with nothing but a Swiss Army knife." Unnatural History,  October, pp. 12-119.

Fleiglehaus, Eric Scotmeister  (1984).  "Tracking wild moss by radio in the African jungle."  Z. Tierpsychol.,  52:12-14.

Galtner, Ashworthy  (1979).  "Use of vacated rodent holes by Central African bluetail monkeys."  Folia Primat.,  31:52-62.

Harrison, Thomas L.  (1981).  "Effects of inbreeding on infant burrowing tendencies in captive guenons at the Frankfurt Zoo."  Nature Review,   50:22-45.

Hicks, T.B.  (1981).  "The fleeing response in four allopatric sub-Saharan cercopithecines and its relation to home range size."  Primates,  22:45-73.

Jernigan, P. Wilkes  (1982).  "Bluetail parasites and other interesting creatures."  Microzoology Review,  12:91-105.

Knuckleberry, Alexander  (1952).  "Population density and biomass of several primate species south of the Ubangi-Congo River system."  Ann. 12th Congress Evol. Soc.,  Vol. IV,  159-220.

Landershot, Albert Prince  (1976).  "Niche separation between Cercopithecus cephus and C. subterraneus."  In Equatorial Forest Mammals  (ed. Marcel Gagneuil).  Paris,  LaFarge Technical Institute Press.

Masters, Arthur Barrett  (1982).  "Congeneric sympatry of Gabonese forest guenons."  Int. J. Primat.,  3:127-154.

Nataka, Bonzai  (1975).  "It's no fun being sick in Africa."  Afr. Trop. Diseases Monthly,  112:29-51.

Ohhohoho, Mitsuo  (1968).  The Professor Mitsuo Ohhohoho Primate Identification Book and African Jungle Survival Guide.  Tokyo,  Edo University Book Binders.

Parkes, B.L., Parkes, C.D., Parkes, H., Parkes, H.H., Parkes, J., Parkes, L.T., Parkes, M., Parkes, M.T., Parkes, R., Parkes, R.E., Parkes, R.E.L., Parkes, S., Parkes, T.T., Parkes, W.E., Parques, Francois and Smith, Basil   (1977).  "Sub-terrestrial foraging of bluetail monkeys at Makokou Study Area, Gabon."  Quart. Review Forest Biol.,  52:1-2.

Preston, T.L. and Keith, Franklin  (1986).  "New data on cercopithecine primates of the Umbugwe."  Centr. Afr. Forest J.,  20:502-597.

Preston, T.L. and Keith, Franklin. Primate Psychology and Aberrant Behavior Patterns.  (In preparation)

Railsback, R. and Foyémé, Mbu  (1986).  Primate Nesting Behavior.   Libreville,  Albert Schweitzer and Co.

Roberts, Letitia P.  (1984).  The Burrowing Guenon of Gabon.  Ontario,  St. Paul's Press.

Shaw, Christopher  (1986).  "Burrow excavation can be a tricky business."  Reader's Digest,  859:79-84.

Spouty, Ralph.  "Hunting the Hell Monkey of Gabon."  Field and Stream,  Dec. 1955,  58-68.

Stilwell, Roger B.  (1969).  "Creation myths among the Fang in the Ogoóué Basin of Gabon."  Central Afr. J. Anthrop.,  27:12-56.

Takahashi, S. and Nishida, R.  (1987).  "Discovery of sub-fossil guenons in Gabonese caves on the Ivindo River." Nature,  325:56-61.

Waters, Delores McKenzie  (1964).  The Week of the Bluetail.  Akron,  Shoestring Press.

Williker-Rogers, Maxine.  "The Bluetail: Yet Another Example of Female Superiority in Nature."  Ms,  Sep. 1972,  23-27.

Williker-Rogers, Maxine  (1973).  "Mobbing behavior of wild bluetail monkeys in Central Africa."  Primates,  14:90-102.