|Proc. Gabon Nature Soc. (1987), 277(3):47-60.|
Burrowing Behavior of Wild Bluetail
Monkeys at the Makokou Study Area, Gabon
Dr. Oondóué M. Boué
Academie Republique Gabonaise
Reginald Pennyworth Maudlin-Jones
Cheltenham-on-Bath Primatology Center
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).
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.
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).
|Fig. 1. Bluetail burrow entrance.||Fig. 2. Bluetail peering out from Iboúnzi vines.|
Juveniles do not have the strength of adults and consequently their burrows are not excavated as deeply. They tend to scrape up fistfuls of decaying leaf matter around the entrances of their burrows to increase the effective dimensions of the nesting space, but even so they are sometimes seen lying on the ground shivering in fright, with only a few twigs to cover them and create the illusion of a burrow.
Burrow construction took place most frequently during the middle part of the day, when other animals could be expected to be resting and inactive. The typical pattern was for the bluetail to creep stealthily out of its burrow, spend about thirty minutes listening and watching for anything that might threaten its safety, then move rapidly to a new location usually at least 100m but not more than 200m away, following which it would spend half an hour making sure it had not been followed. Only then would actual digging commence.
In 89.3% of observed burrow excavations, bluetails approached their chosen site rearwards, using their powerful tarsier-like legs and clawed feet (Atherington, 1981) to scoop out the beginnings of the burrow while remaining alert for any noise or movement in the surrounding forest. Only when the burrow was deep enough to conceal themselves in did they reverse their position and continue digging with their hands. Time of construction normally was approximately two hours, although it ranged from a minimum of 50 minutes in the case of one particularly nervous individual to a maximum of several days when the burrow walls kept caving in or when the ground was especially hard.
Once the excavation has been completed, bluetails line their nests inside with mosses and birdclaw ferns which they customarily steal in surreptitious raids on neighboring burrows. It frequently occurs that when they are out on these raids, other bluetails are stealing their nesting materials. By attaching a transmitter to a particularly attractive clump of moss, the German primatologist Eric Scotmeister Fleiglehaus was able to document its appearance in the burrows of nine different bluetails in a period of just twenty-two minutes.
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.
Mean daily hours spent in burrows
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
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.
Furthermore, no degree of habituation was achieved over the nineteen year period, and C. subterraneus target animals appeared to be just as nervous and scared at the presence of observers at the conclusion of the study as at its inception.
Of course, while observing animals in the wild, it is very difficult to attribute any particular behavior to specific emotional states such as fear without anthropomorphising the subjects. But certain behavioral traits in bluetails have
Fig. 3. Bluetails frantically searching for their burrows
in an area of recently cleared vine forest.
been commonly observed which seem to evidence fear or something like it. Of 862 incidents in which an observer happened upon a bluetail in the forest, in 790 cases the bluetail's eyes widened measurably and the lips were drawn back in what was taken to be a grimace of fear. Teeth were heard clacking at distances of up to 50 meters in 527 instances. The ducking of the head has been well-observed and described elsewhere (Bongo, 1980), and it will suffice to say here that it is widely practised and is probably a defensive tactic. Their most amazing behavior of all is their ability to suck in their stomachs in order to appear scrawny and not worth a predator's trouble. When they are startled, bluetails at least 70% of the time will automatically deflate their stomachs and lie about on the ground looking pathetic (Boué, 1986). In other cases, if their burrow is not nearby, the bluetail will attempt to hide under a large leaf.
There is also fossil evidence of a severe population decline since the Pleistocene when bluetail guenons were the most prolific and wide-ranging species of their genus, and there would not seem to be any way that their population could have been so large and they so reproductively successful had they followed their present behavioral patterns. Not only is there no other guenon that burrows, there is no other primate that burrows. In fact, burrowing goes against most of what a primate is. There is nothing in the fossil record that indicates that primates have ever burrowed. Therefore, it appears that C. subterraneus has colonized a niche that is totally inappropriate for its taxa, based on 60 million years of primate evolution. But however inappropriate, this behavior could still be shown to be adaptive if it conveyed some advantage to the individual concerned, or to the group as a whole, either for survival or reproduction. We were unable to document such an advantage. To the contrary, the disadvantages are numerous, as has already been outlined.
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.
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.
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