I. Geoffroy, 1851
General characteristics
The genus Hapalemur is easily distinguished from the other genera of the family Lemuridae. The body size is similar or smaller than Lemur and Eulemur, but the skull is very different, being more round, with a large face and a short muzzle. The fur is reddish gray, more or less tinged with green. The round-like ears are hidden in the fur. Just like the other Lemuridae, they run with great agility on branches. These animals mainly have crepuscular habits. They live in forests that are rich in bamboo and they can generally be found in little groups of 2 – 5 individuals. Their calls are rather various and they have very well developed cutaneous marking glands that are situated on the arms. Like Lemur, they have only one pair of mammae.
Systematics
Classically two species are distinguished: Hapalemur griseus (Link) and Hapalemur simus Gray. For the second species Pocock, 1917 and Gray, 1870, proposed to raise a new genus Prolemur. However, their similarities appeared to be sufficient to maintain them in the same genus Hapalemur.
Hapalemur simus, a very rare species, was only known from some museum specimens until 1972 and it was considered that this animal did not possess branchial and antebrachial glands. The observation and capture realized by Peyriéras and Petter in 1972 showed that the males possess these glandular differentiations, but arranged in a different way than in H. griseus. These glands oppose each other when the arm is bent, but with H. simus their position on the arms is directly proximal to the elbow joint.
Two subspecies or very similar species were described for Hapalemur griseus, which differ in color: H. g. griseus (Link, 1795) with a yellowish gray fur, and H. g. olivaceus (I. Geoffroy, 1851) with an olive-gray and russet fur. The individual variability of the color of this species is large, depending on the state of the fur of preserved specimens. Only after study of numerous collections and examination of the type material, it was until today impossible to consider these differences as substantial. I. Geoffroy Saint-Hilaire, who erected the second taxon at the species level, was not sure himself when he made the description: "There remains some doubt for me, and this species is one of those of which I should have postponed its publication without the necessary and complete listing of the collections in the catalog". He noticed that the H. griseus type specimen collected by Sonnerat, was already in a bad state at that time. This type is still in the collections of the MNHN in Paris, but the skull is absent. It is most likely an animal that has been living in captivity for a rather long time. Its fur is seriously ruined. It has lost the speckled green hairs that are characteristic for Hapalemur and has less than only soft sandy-gray hair.
The type specimen of H. g. olivaceus is rather well preserved. It is of similar size as the specimen of H. g. griseus, but has a rather nice pelage. Geoffroy writes on this subject: "I would not have admitted that H. olivaceus is a distinct species if I had only known its external characteristics, however, several internal characteristics are concordant with these. The posterior part of the lower jaw of H. olivaceus is remarkably different". Unfortunately, the skull of this specimen is not in the collections of the museum (MNHN) anymore. The skull is registered in the type inventory of the museum that was made by P. Rode, 1939: 438, No 132), but is absent from the collection since 1942. It is therefore impossible to specify the differences that I. Geoffroy Saint-Hilaire has not described in detail. Schlegel and Pollen, 1868 have not recognized the validity of the species, and J.E. Gray, 1870 also had his doubts, in contrast to Schwarz, 1931 and Hill, 1953.
The two species were displayed on color plates in the Histoire physique, naturelle et politique de Madagascar published by A. Grandidier, 1875. There appeared to be a faint difference on those plates between H. g. griseus and H. g. olivaceus, and it is likely that no other document than the figures of the types were used for the distinction of the subspecies.
A skeptical attitude seems to be the wisest while waiting for new documentation. Observations of specimens of H. griseus from the same region generally makes it possible to see small differences in the shape of the head, the width of the face or the distance between the eyes. A rather large individual variation is present within the species, which is, however, less evident from the dry skins in museums.
The exact origin of Hapalemur simus was not known and a mission (Petter and Pariente) was organized in 1968, based on information from Webb, 1929, hoping to find this animal in the vegetation around Lac Alaotra. The members of the expedition had never seen this animal alive. A Hapalemur of larger size than H. griseus was seen there, so the existence of H. simus at this location seemed possible. In fact, it was another Hapalemur, as was proved with captures.
The hapalemurs of Lac Alaotra are Hapalemur griseus of larger body size (almost double) and it is easy to notice their big head and thick fur of darker color than H. g. griseus, only by floating along in pirogue at the lake. However, fishermen had noticed an animal with a brighter pelage among them from time to time.
This form has a different ecology than H. g. griseus and was proposed to be named Hapalemur griseus alaotrensis Petter et al., 1977.
It is interesting to remark that a hybrid between H. g. griseus and H. g. alaotrensis was bred in the Laboratoire d’Ecologie du Muséum national d’Histoire at Brunoy in 1969, as well as in the Laboratoire de Zoologie de l’ORSTOM at Tananarive in 1972 and 1973.
A third form was simply recognized by its genetic formula (2N = 58 instead of 2N = 54) by J. Buettner-Janusch et al., 1966, which was wrongly identified as H. g. olivaeus. It shows a close resemblance to H. g. griseus. Its color is slightly paler and it lives in the Northwest and West. It is named Hapalemur griseus occidentalis by Rumpler, 1975.
Within several years other forms of Hapalemur griseus have been found that are more or less considered as subspecies: H. g. alaotrensis (near the Lac Aloatra), H. g. occidentalis, H. g. meridionalis (Karyo H. g. meridionalis), and H. aureus. Moreover, H. simus could be localized. It is obvious that there is a great variety within the genus and it seems possible that other local forms still could be discovered.
The research that was carried out mainly by the team of Y. Rumpler permitted to compare all the forms genetically and to propose the phylogeny of the group.
When H. aureus was discovered by Meier et al., 1987, it was presented as a new species based on its very distinct external characteristics. A preliminary cytogenetic study (Rumpler et al., 1988) showed that the karyotype differed from the other Hapalemur by a chromosomal rearrangement that permitted to predict problems during the meiosis leading to sterile hybrids (Ratomponirina et al., 1988). With all the Hapalemur species (Rumpler and Dutrillaux, 1978; Warter et al., 1987) a phylogenetic tree was constructed that permitted to find the branching point of H. aureus.
A comparison of the karyotype of H. aureus with that of other Hapalemur species has demonstrated that the karyotype of Hapalemur comprises many acrocentric chromosomes and that in H. g. occidentalis are also present in all H. griseus, and are absent in H. aureus. In the latter species, these two metacentric chromosomes are replaced by acrocentric chromosomes. It seems likely that these chromosomes stem from the acrocentric ones of H. griseus by two rearrangements.
DNA research has confirmed the evolutionary tree that was based on chromosome rearrangements, affirming the specific status of H. aureus.
Systematics of the genus
A Hapalemur griseus (Link, 1795)
Lemur griseus Link, 1795, Beytr. Naturg., 1, 2 Stück, p. 65 (1)
Type: a specimen collected by Sonnerat (Muséum National d'Histoire Naturelle, Paris).
H. griseus has a gray-russet coat that is more or less green tinted. The coat is rather variable depending on the age, the health state of the animal or the conditions during captivity.
At least three subspecies can be distinguished of which two are differentiated only by size and ecology.
– H. g. alaotrenensis is 40 cm tall (body and head) and has a tail of about 40 cm. The coat is generally darkly tinted compared to the subspecies mentioned below. Diploid number 2N = 54.
– H. g. griseus and H. g. occidentalis are both 25 - 30 cm tall (head and body) and have a tail that is slightly longer than the body. Diploid number 2N = 54.
– H. g. occidentalis has a coat that is slightly more pale than the nominative subspecies; the face is somewhat longer. Diploid number 2N = 58.
a) Hapalemur griseus griseus (Link, 1795)
Synonyms: cinereus Desmarest, 1820; olivaceus I. Geoffroy, 1821; schlegeli Pocock, 1917.
Malagasy names:
Bokombolo (name given by the Betsinisaraka in the Northeast; bokom would be an imitation of the call, bolo comes from bolo = bamboo);
Kotrika (name given by the Betsimisaraka in the Périnet region; imitation of the call).
b) Hapalemur griseus alaotrensis Petter et al., 1977
Holotype: Eastern Madagascar, Lac Alaotra (J.-J. Petter) (Catalogue général, Magasin de Mammalogie et d'Ornithologie du Muséum national d'Histoire naturelle, Paris, 1975; no 1122)
Malagasy name: Bandro (name used in the region of the Lac Alaotra).
Syntype: Western Madagascar (Collection of the Institute de la Recherche scientifique et technique, Tananarive - Tsimbazaza).
c) Hapalemur griseus occidentalis Rumpler, 1975
Hapalemur griseus occidentalis Rumpler, 1975. In: Lemur Biology, Plenum Press, NY.
Malagasy names:
Bekola (allusion at the armpit gland, that resembles a large ganglion);
Kofi (imitation of the call). Both these names are used in the Antsalova region, western Madagascar.
B Hapalemur simus Gray, 1870
Hapalemur simus Gray, 1870. Cat. Monkeys, Lemurs and Fruit-eating Bats in British Museum, p. 133: Proc. Zool. London, 1870, p. 828, fig. 1 to 4, pl. LII.
H. simus is of much larger size than the other Hapalemur species and similar to the size of Lemur. H. simus has a body size of about 45 cm and a weight of 2.5 kg. The pelage has a brown-green color with on top of the head and the upper part of the back a more red and darker color, and an ochre spot at the sacral region. The tail has the same color as the body but the end is brown-black. The hairs are gray at the base and they tint from brown-green, brown-yellow to brown-black towards the end, which often gives the pelage a shining appearance, if the animal is in good health. This particular coloration of the hair also exists with certain Eulemur species, but seems more emphasized with this species.
C Hapalemur aureus Meier et al., 1987
Hapalemur aureus Meier, B., Albignac, R., Peyriéras, A., Rumpler, Y., and Wright, P., 1987. A new species of Hapalemur (Primates) from South East Madagascar (with 1 color plate). Folia Primatologica 48: 211-215.
H. aureus has an intermediate size between H. griseus and H. simus. The face is black, surrounded by luxuriant golden-yellow eyebrows, cheeks and throat. The ventral part of the body is yellow and the dorsal part of the body has gray-brown guard hairs with pale orange underfur. There is no dichromatism between the male and the female. The female is somewhat grayer on the back.
Long-term observations in the Ranomafana forest (Meier, Albignac, Peyriéras, Rumpler, and Wright) made it possible to follow for seven months in 1986 – 1987 several groups and clearly study the interspecific relationships between H. griseus, H. simus and H. aureus, which live in each others neighborhood. In times past, these three species probably lived together over a large part of eastern Madagascar.