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Brief Report
Folia Primatol 2000;71:422–425
Lemur Origins: Rafting by Groups of
Hibernators?
Peter M. Kappeler
Abteilung Verhaltensforschung/Ökologie, Deutsches Primatenzentrum,
Göttingen, Deutschland
Received: February 9, 2000
Accepted after revision: May 23, 2000
Peter M. Kappeler
Abteilung Verhaltensforschung/Ökologie
Deutsches Primatenzentrum, Kellnerweg 4
D–37077 Göttingen (Germany)
E-Mail pkappel@gwdg.de
ABC
Fax + 41 61 306 12 34
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© 2001 S. Karger AG, Basel
0015–5713/00/0716–0422$17.50/0
Accessible online at:
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Key Words
Primate evolution
W Lemurs W Madagascar W Biogeography
Introduction
When and how non-human primates first arrived on Madagascar remains one of
the most enigmatic questions in primate evolution [1–3]. Madagascar broke away from
the African mainland and India long before the estimated origin of the first primates
[4–7]. Because African and Asian lorises are the closest living relatives of Malagasy
primates, however, some of their common ancestors must have migrated to distant
islands or continents. Recent phylogenetic analyses strongly indicate an African origin
for lemurs and lorises, thereby supporting a primate colonisation of Madagascar from
Africa [8], but proposed mechanisms for this transoceanic colonisation have been highly
controversial. Here I cite evidence from several recent studies that suggest a likely
mechanism for a successful colonisation across the formidable water barrier of the
Mozambique Channel.
Three hypotheses have been proposed to explain the presence of primates and ter-
restrial mammals on Madagascar long after its separation from Africa: (1) island-hop-
ping across the Mozambique Channel after a temporary reduction in sea levels [9],
(2) invasion during the presence of a temporary land bridge [10] and (3) rafting on
drifting vegetation [11, 12]. The geological evidence concerning the presence of a chain
of islands or even a continuous land bridge during these periods is still incomplete and
controversial [7, 10]. Moreover, the first two hypotheses fail to provide a satisfactory
explanation for the small number of terrestrial mammalian taxa that successfully colon-
ised Madagascar. The rafting hypothesis has been dismissed on the grounds that lemurs
and other small mammals were not physiologically suited for a successful crossing of the
Lemur Origins
Folia Primatol 2000;71:422–425
423
more than 400 km wide channel [3, 10, 13], but successful over-water dispersal is highly
probable over geological times [14] and has been confirmed for other vertebrates [15,
16].
The Extended Rafting Hypothesis
Several independent studies recently provided pieces of evidence relevant for the
reconstruction of the primate colonisation of Madagascar and suggest a plausible mech-
anism for successful rafting. First, phylogenetic analyses of mitochondrial DNA
sequences and an extensive morphological data set demonstrated a single origin for
Malagasy primates [8], followed by rapid cladogenesis, which makes a single successful
colonisation event sufficient to explain the present distribution and diversity of lemurs.
Second, a composite estimate of primate phylogeny suggested that the mouse and dwarf
lemurs (Cheirogaleidae) are the most ancestral group among the living lemurs [17].
Third, mouse (Microcebus spp.) and dwarf (Cheirogaleus spp.) lemurs have long
been known to enter daily torpor or month-long hibernation during the cool austral
summer [18–20, see also 21, 22]. Recent physiological studies in the field demon-
strated that these lemurs actually reduce their metabolic rates by up to 90% and lower
their body temperatures close to ambient temperatures, thereby saving around 40% of
their average daily energy expenditure [23]. Finally, field studies of individually
marked cheirogaleids revealed that mouse and dwarf lemurs typically spend daily and
seasonal periods of inactivity in aggregations of up to 15 individuals in single tree holes
[24, 25, see also 26, 27], thereby further enhancing their energy savings [28]. Because of
the phylogenetic position of these taxa, it is most parsimonious to assume that this
combination of behavioural and physiological traits was also shared by the ancestral
lemurs [12].
Together, the results of these studies provide indirect evidence for the rafting
hypothesis for the primate colonisation of Madagascar by suggesting a plausible mecha-
nism for a successful migration. Accordingly, it is less likely that ‘a pop-eyed ancestral
lemur clung with all its hands onto the wave-washed twigs of a raft of floating tree trunks
or tangled branches’ [11, see also 13], but rather that entire groups of animals survived
the weeks [16] or even months of such a journey without food and water sleeping in a
hollow tree while rafting across the sea. Moreover, according to this scenario the initial
demographic and genetic bottleneck would have been much wider because of the arrival
of several individuals at the same place and time, making a successful colonisation
much more likely.
Successful rafting of more or less inactive individuals could also explain the pres-
ence of other major mammalian groups on Madagascar. The insectivores of the family
Tenrecidae have low metabolic rates and several of them hibernate for months [29].
Similarly, some Herpestidae and Viverridae are among the most hypometabolic carni-
vores [30]. The physiological traits exhibited by these unrelated taxa may have been
advantageous during extended voyages across open seas, thereby explaining a large pro-
portion of the composition of today’s mammalian community on Madagascar. In addi-
tion, the Asian lorises, which must have also originated in Africa [31, 32], have some of
the lowest metabolic rates among primates [33], suggesting the possibility that their
ancestors may have reached Asia also by rafting. A recent phylogenetic analysis, how-
ever, suggested an Asian origin for Madagascar’s endemic rodents, followed by a subse-
424
Folia Primatol 2000;71:422–425
Kappeler
quent secondary invasion of Africa [34], indicating that the Eocene exchange of mam-
mals among Africa, Asia and Madagascar was not limited to one particular direction
[35].
Acknowledgments
I thank Nick Davies, Steve Goodman, Carola Borries, Eckhard Heymann and Caroline Harcourt
for stimulating discussions, helpful suggestions and for their comments on an earlier version of the
manuscript.
References
1 Fleagle JG: Primate Adaptation and Evolution. New York, Academic Press, 1998.
2 Martin RD: Primate Origins and Evolution. London, Chapman & Hall, 1990.
3 Simons EL: Lemurs: Old and new; in Goodman S, Patterson B (eds): Natural Change and Human Impact in
Madagascar. Washington, Smithsonian Press, 1997, pp 142–166.
4 Rabinowitz P, Covin M, Falvey D: The separation of Madagascar and Africa. Science 1983;220:67–69.
5 Storey M, Mahoney J, Saunders A, Duncan R, Kelley S, Coffin M: Timing of hot spot-related volcanism and the
breakup of Madagascar and India. Science 1995;267:852–855.
6 Martin RD: Primate origins: Plugging the gaps. Nature 1993;363:223–234.
7 Krause D, Hartman J, Wells A: Late cretaceous vertebrates from Madagascar: Implications for biotic change in
deep time; in Goodman S, Patterson B (eds): Natural Change and Human Impact in Madagascar. Washington,
Smithsonian Institution Press, 1997, pp 3–43.
8 Yoder A, Cartmill M, Ruvolo M, Smith K, Vilgalys R: Ancient single origin for Malagasy primates. Proc Natl
Acad Sci USA 1996;93:5122–5126.
9 Tattersall I: The Primates of Madagascar. New York, Columbia University Press, 1982.
10 McCall R: Implications of recent geological investigations of the Mozambique Channel for the mammalian
colonization of Madagascar. Proc R Soc Lond B 1997;264:663–665.
11 Jolly A: A World Like Our Own. New Haven, Yale University Press, 1980.
12 Warren RD, Crompton RH: Lazy leapers: Energetics, phylogenetic inertia and the locomotor differentiation of
the Malagasy primates; in Lourenco W (ed): Biogéographie de Madagascar. Paris, ORSTOM, 1996, pp 259–
266.
13 Simons EL: The fossil record of primate phylogeny; in Goodman M, Tashian R, Tashian J (eds): Molecular
Anthropology. New York, Plenum Press, 1976, pp 35–62.
14 Simpson GG: Probabilities of dispersal in geologic time. Bull Am Mus Nat Hist 1952;99:163–176.
15 Censky E, Hodge K, Dudley J: Over-water dispersal of lizards due to hurricanes. Nature 1998;395:556.
16 Houle A: Floating islands: A mode of long-distance dispersal for small and medium-sized terrestrial vertebrates.
Divers Distrib 1998;4:201–216.
17 Purvis A: A composite estimate of primate phylogeny. Philos Trans R Soc Lond B 1995;348:405–421.
18 Petter JJ: Ecological and behavioral studies of Madagascar lemurs in the field. Ann N Y Acad Sci 1962;102:
267–281.
19 Bourlière F, Petter-Rousseaux A: Existence probable d’un rythme métabolique saisonnier chez les Cheirogalei-
nae (Lemuroidea). Folia Primatol 1966;4:249–256.
20 Petter-Rousseaux A: Seasonal activity rhythms, reproduction, and body weight variations in five sympatric
nocturnal prosimians in simulated light and climatic conditions; in Charles-Dominique P, Cooper HM, Hladik
A, Hladik CM, Pages E, Pariente GF, Petter-Rousseaux A, Petter J-J, Schilling A (eds): Nocturnal Malagasy
Primates: Ecology, Physiology and Behavior. New York, Academic Press, 1980, pp 137–152.
21 Atsalis S: Seasonal fluctations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus
rufus. Int J Primatol 1999;20:883–910.
22 Schmid J, Kappeler PM: Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the
gray mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 1998;43:125–132.
23 Ortmann S, Heldmaier G, Schmid J, Ganzhorn JU: Spontaneous daily torpor in Malagasy mouse lemurs.
Naturwissenschaften 1997;84:28–32.
24 Fietz J: Monogamy as a rule rather than exception in nocturnal lemurs: The case of the fat-tailed dwarf lemur,
Cheirogaleus medius. Ethology 1999;105:259–272.
25 Radespiel U, Cepok S, Zietemann V, Zimmermann E: Sex-specific usage patterns of sleeping sites in grey mouse
lemurs (Microcebus murinus) in Northwestern Madagascar. Am J Primatol 1998;46:77–84.
Lemur Origins
Folia Primatol 2000;71:422–425
425
26 Petter J-J: Contribution à l’étude du Cheirogaleus medius dans la forêt de Morondava; in Rakotovao L, Barre V,
Sayer J (eds): L’équilibre des écosystèmes forestiers à Madagascar: actes d’un séminaire international. Cam-
bridge, Page Bros Ltd, 1988, pp 57–60.
27 Martin RD: A preliminary field-study of the lesser mouse lemur (Microcebus murinus J.F. Miller 1977). Z
Tierpsychol Suppl 1972;9:43–89.
28 Perret M: Energetic advantage of nest-sharing in a solitary primate, the lesser mouse lemur (Microcebus muri-
nus ). J Mammal 1998;79:1093–1102.
29 Stephenson PJ, Racey PA: Reproductive energetics of the Tenrecidae (Mammalia: Insectivora). II. The shrew-
tenrecs, Microgale spp. Physiol Zool 1993;66:664–685.
30 McNab B: Basal rate of metabolism, body size, and food habits in the order Carnivora; in Gittleman J (eds):
Carnivore Behavior, Ecology, and Evolution. Ithaca, Cornell University Press, 1989, pp 335–354.
31 Charles-Dominique P, Martin RD: Evolution of lorises and lemurs. Nature 1970;227:257–260.
32 Rasmussen DT, Nekaris KA: Evolutionary history of lorisiform primates. Folia Primatol 1998;69:250–285.
33 Rasmussen DT, Izard MK: Scaling of growth and life history traits relative to body size, brain size, and metabol-
ic rate in lorises and galagos (Lorisidae, Primates). Am J Phys Anthropol 1988;75:357–367.
34 Jansa S, Goodman S, Tucker P: Molecular phylogeny and biogeography of the native rodents of Madagascar
(Muridae: Nesomyinae): A test of the single-origin hypothesis. Cladistics 1999;15:253–270.
35 Masters J, Rayner R, Tattersall I: Pattern and process in strepsirhine phylogeny; in Alterman L, Doyle G, Izard
M (eds): Creatures of the Dark. New York, Plenum Press, 1995, pp 31–44.